3D bioprinted silk fibroin hydrogels for tissue engineering

Soon Hee Kim, Heesun Hong, Olatunji Ajiteru, Md. Tipu Sultan, Young Jin Lee, Ji Seung Lee, Ok Joo Lee, Hanna Lee, Hae Sang Park, Kyu Young Choi, Joong Seob Lee, Hyung Woo Ju, In-Sun Hong, Chan Hum Park

Published: 2021-10-28 DOI: 10.1038/s41596-021-00622-1

tissue engineering

silk fibroin hydrogels

3D bioprinting

methacrylated bioink

biocompatibility

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The development of biocompatible and precisely printable bioink addresses the growing demand for three-dimensional (3D) bioprinting applications in the field of tissue engineering. We developed a methacrylated photocurable silk fibroin (SF) bioink for dig
Introduction
Materials for Procedure 1
Procedure 1: fabrication of Sil-MA bioink and hydrogel and characterization
Materials for Procedure 2
Procedure 2: trachea tissue engineering using Sil-MA hydrogel
Troubleshooting
Timing
Anticipated results
References
ACKNOWLEDGMENTS

Oliveira, J. M. et al. Current and future trends of silk fibroin-based bioinks in 3D printing. J. 3D Print. Med. 4, 69–73 (2020).
Ng, W. L., Chua, C. K. & Shen, Y.-F. Print me an organ! Why we are not there yet. Prog. Polym. Sci. 97, 101145 (2019).
Matai, I., Kaur, G., Seyedsalehi, A., McClinton, A. & Laurencin, C. T. Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials 226, 119536 (2020).
Mandrycky, C., Wang, Z., Kim, K. & Kim, D.-H. 3D bioprinting for engineering complex tissues. Biotechnol. Adv. 34, 422–434 (2016).
Axpe, E. & Oyen, M. L. Applications of alginate-based bioinks in 3D bioprinting. Int. J. Mol. Sci. 17, 1976 (2016).
Shao, Z. & Vollrath, F. Surprising strength of silkworm silk. Nature 418, 741–741 (2002).
Müller, M., Becher, J., Schnabelrauch, M. & Zenobi-Wong, M. Nanostructured pluronic hydrogels as bioinks for 3D bioprinting. Biofabrication 7, 035006 (2015).
Wang, Z. et al. A simple and high-resolution stereolithography-based 3D bioprinting system using visible light crosslinkable bioinks. Biofabrication 7, 045009 (2015).
Takagi, D. et al. High-precision three-dimensional inkjet technology for live cell bioprinting. Int. J. Bioprinting 5, 208 (2019).
Ng, W. L., Lee, J. M., Yeong, W. Y. & Naing, M. W. Microvalve-based bioprinting–process, bio-inks and applications. Biomater. Sci. 5, 632–647 (2017).
Guillotin, B. et al. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 31, 7250–7256 (2010).
Ozbolat, I. T. & Hospodiuk, M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials 76, 321–343 (2016).
Gupta, S. et al. Evaluation of silk‐based bioink during pre and post 3D bioprinting: a review. J. Biomed. Mater. Res. B Appl. Biomater. 109, 279–293 (2021).
Singh, Y. P., Bandyopadhyay, A. & Mandal, B. B. 3D bioprinting using cross-linker-free silk–gelatin bioink for cartilage tissue engineering. ACS Appl. Mater. Interfaces 11, 33684–33696 (2019).
Ng, W. L. et al. Vat polymerization-based bioprinting—process, materials, applications and regulatory challenges. Biofabrication 12, 022001 (2020).
Zhang, J., Hu, Q., Wang, S., Tao, J. & Gou, M. Digital light processing based three-dimensional printing for medical applications. Int. J. Bioprinting 6, 242 (2020).
Wu, C., Wang, B., Zhang, C., Wysk, R. A. & Chen, Y.-W. Bioprinting: an assessment based on manufacturing readiness levels. Crit. Rev. Biotechnol. 37, 333–354 (2017).
Kim, S. H. et al. Precisely printable and biocompatible silk fibroin bioink for digital light processing 3D printing. Nat. Commun. 9, 1620 (2018).
Lu, Y., Mapili, G., Suhali, G., Chen, S. & Roy, K. A digital micro‐mirror device‐based system for the microfabrication of complex, spatially patterned tissue engineering scaffolds. J. Biomed. Mater. Res. A 77, 396–405 (2006).
Zhu, W. et al. 3D printing of functional biomaterials for tissue engineering. Curr. Opin. Biotechnol. 40, 103–112 (2016).
Grogan, S. P. et al. Digital micromirror device projection printing system for meniscus tissue engineering. Acta Biomater. 9, 7218–7226 (2013).
Lin, H. et al. Application of visible light-based projection stereolithography for live cell-scaffold fabrication with designed architecture. Biomaterials 34, 331–339 (2013).
Lam, T. et al. Photopolymerizable gelatin and hyaluronic acid for stereolithographic 3D bioprinting of tissue‐engineered cartilage. J. Biomed. Mater. Res. B Appl. Biomater. 107, 2649–2657 (2019).
Soman, P., Chung, P. H., Zhang, A. P. & Chen, S. Digital microfabrication of user‐defined 3D microstructures in cell‐laden hydrogels. Biotechnol. Bioeng. 110, 3038–3047 (2013).
Zhang, A. P. et al. Rapid fabrication of complex 3D extracellular microenvironments by dynamic optical projection stereolithography. Adv. Mater. 24, 4266–4270 (2012).
Melke, J., Midha, S., Ghosh, S., Ito, K. & Hofmann, S. Silk fibroin as biomaterial for bone tissue engineering. Acta Biomater. 31, 1–16 (2016).
Ju, H. W. et al. Silk fibroin based hydrogel for regeneration of burn induced wounds. Tissue Eng. Regen. Med. 11, 203–210 (2014).
Qi, Y. et al. A review of structure construction of silk fibroin biomaterials from single structures to multi-level structures. Int. J. Mol. Sci. 18, 237 (2017).
Kim, S. H., Kim, D. Y., Lim, T. H. & Park, C. H. Silk fibroin bioinks for digital light processing (DLP) 3D bioprinting. Adv. Exp. Med. Biol. 1249, 53–66 (2020).
Kambe, Y. et al. Beta-sheet content significantly correlates with the biodegradation time of silk fibroin hydrogels showing a wide range of compressive modulus. Polym. Degrad. Stab. 179, 109240 (2020).
Cao, Z., Chen, X., Yao, J., Huang, L. & Shao, Z. The preparation of regenerated silk fibroin microspheres. Soft Matter 3, 910–915 (2007).
Sheikh, F. A. et al. 3D electrospun silk fibroin nanofibers for fabrication of artificial skin. Nanomed. Nanotechnol. Biol. Med. 11, 681–691 (2015).
Lee, J. M. et al. Artificial auricular cartilage using silk fibroin and polyvinyl alcohol hydrogel. Int. J. Mol. Sci. 18, 1707 (2017).
Kim, J.-H. et al. Osteoinductive silk fibroin/titanium dioxide/hydroxyapatite hybrid scaffold for bone tissue engineering. Int. J. Biol. Macromol. 82, 160–167 (2016).
Chung, E. J., Ju, H. W., Park, H. J. & Park, C. H. Three‐layered scaffolds for artificial esophagus using poly (ɛ‐caprolactone) nanofibers and silk fibroin: An experimental study in a rat model. J. Biomed. Mater. Res. A 103, 2057–2065 (2015).
Lee, M. C. et al. Fabrication of silk fibroin film using centrifugal casting technique for corneal tissue engineering. J. Biomed. Mater. Res. B Appl. Biomater. 104, 508–514 (2016).
Hong, H. et al. Digital light processing 3D printed silk fibroin hydrogel for cartilage tissue engineering. Biomaterials 232, 119679 (2020).
Wang, Q., Han, G., Yan, S. & Zhang, Q. 3D printing of silk fibroin for biomedical applications. Materials 12, 504 (2019).
Das, S. et al. Bioprintable, cell-laden silk fibroin–gelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs. Acta Biomater. 11, 233–246 (2015).
Shi, W. et al. Structurally and functionally optimized silk‐fibroin–gelatin scaffold using 3D printing to repair cartilage injury in vitro and in vivo. Adv. Mater. 29, 1701089 (2017).
Sharma, A. 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. 5, 1518–1533 (2019).
Mehrotra, S. et al. Nonmulberry silk based ink for fabricating mechanically robust cardiac patches and endothelialized myocardium‐on‐a‐chip application. Adv. Funct. Mater. 30, 1907436 (2020).
Zheng, Z. et al. 3D bioprinting of self‐standing silk‐based bioink. Adv. Healthc. Mater. 7, 1701026 (2018).
Nguyễn, T.T., Ratanavaraporn, J. & Yodmuang, S. Alginate-silk fibroin bioink: a printable hydrogel for tissue engineering. in 2019 12th Biomedical Engineering International Conference (BMEiCON) 1–4 (IEEE, 2019).
Compaan, A. M., Christensen, K. & Huang, Y. Inkjet bioprinting of 3D silk fibroin cellular constructs using sacrificial alginate. ACS Biomater. Sci. Eng. 3, 1519–1526 (2017).
Jiang, J.-P. et al. Three-dimensional bioprinting collagen/silk fibroin scaffold combined with neural stem cells promotes nerve regeneration after spinal cord injury. Neural Regen. Res. 15, 959 (2020).
Lee, H. et al. Fabrication of micro/nanoporous collagen/dECM/silk-fibroin biocomposite scaffolds using a low temperature 3D printing process for bone tissue regeneration. Mater. Sci. Eng. C. 84, 140–147 (2018).
Na, K. et al. Effect of solution viscosity on retardation of cell sedimentation in DLP 3D printing of gelatin methacrylate/silk fibroin bioink. J. Ind. Eng. Chem. 61, 340–347 (2018).
Kwak, H., Shin, S., Lee, H. & Hyun, J. Formation of a keratin layer with silk fibroin-polyethylene glycol composite hydrogel fabricated by digital light processing 3D printing. J. Ind. Eng. Chem. 72, 232–240 (2019).
Shin, S., Kwak, H. & Hyun, J. Melanin nanoparticle-incorporated silk fibroin hydrogels for the enhancement of printing resolution in 3D-projection stereolithography of poly (ethylene glycol)-tetraacrylate bio-ink. ACS Appl. Mater. Interfaces 10, 23573–23582 (2018).
Lee, H., Shin, D., Shin, S. & Hyun, J. Effect of gelatin on dimensional stability of silk fibroin hydrogel structures fabricated by digital light processing 3D printing. J. Ind. Eng. Chem. 89, 119–127 (2020).
Piluso, S. et al. Rapid and cytocompatible cell-laden silk hydrogel formation via riboflavin-mediated crosslinking. J. Mater. Chem. B 8, 9566–9575 (2020).
Lee, O. J. et al. Biodegradation behavior of silk fibroin membranes in repairing tympanic membrane perforations. J. Biomed. Mater. Res. A 100, 2018–2026 (2012).
Yoshimizu, H. & Asakura, T. Preparation and characterization of silk fibroin powder and its application to enzyme immobilization. J. Appl. Polym. Sci. 40, 127–134 (1990).
Park, Y. R. et al. Three-dimensional electrospun silk-fibroin nanofiber for skin tissue engineering. Int. J. Biol. Macromol. 93, 1567–1574 (2016).
Park, H. J. et al. Fabrication of 3D porous silk scaffolds by particulate (salt/sucrose) leaching for bone tissue reconstruction. Int. J. Biol. Macromol. 78, 215–223 (2015).
Irawan, V., Sung, T.-C., Higuchi, A. & Ikoma, T. Collagen scaffolds in cartilage tissue engineering and relevant approaches for future development. Tissue Eng. Regen. Med. 15, 673–697 (2018).
Miyaguchi, Y. & Hu, J. Physicochemical properties of silk fibroin after solubilization using calcium chloride with or without ethanol. Food Sci. Technol. Res. 11, 37–42 (2005).
Zhang, X., Reagan, M. R. & Kaplan, D. L. Electrospun silk biomaterial scaffolds for regenerative medicine. Adv. Drug Deliv. Rev. 61, 988–1006 (2009).
Tao, H. et al. Inkjet printing of regenerated silk fibroin: from printable forms to printable functions. Adv. Mater. 27, 4273–4279 (2015).
Sashina, E., Bochek, A., Novoselov, N. & Kirichenko, D. Structure and solubility of natural silk fibroin. Russ. J. Appl. Chem. 79, 869–876 (2006).
Gulrez, S. K. H., Al-Assaf, S. & Phillips, G. O. Hydrogels: methods of preparation, characterisation and applications. in Progress in Molecular and Environmental Bioengineering: From Analysis and Modeling to Technology Applications, 117–150 (IntechOpen, 2011).
Nguyen, T. P. et al. Silk fibroin-based biomaterials for biomedical applications: a review. Polymers 11, 1933 (2019).
Sun, M. et al. Synthesis and properties of gelatin methacryloyl (GelMA) hydrogels and their recent applications in load-bearing tissue. Polymers 10, 1290 (2018).
Reis, A. V. et al. Reaction of glycidyl methacrylate at the hydroxyl and carboxylic groups of poly (vinyl alcohol) and poly (acrylic acid): is this reaction mechanism still unclear? J. Org. Chem. 74, 3750–3757 (2009).
Wang, Z., Jin, X., Dai, R., Holzman, J. F. & Kim, K. An ultrafast hydrogel photocrosslinking method for direct laser bioprinting. RSC Adv. 6, 21099–21104 (2016).
Vashist, A. et al. Bioresponsive injectable hydrogels for on-demand drug release and tissue engineering. Curr. Pharm. Des. 23, 3595–3602 (2017).
Kim, S. H. et al. Rapidly photocurable silk fibroin sealant for clinical applications. NPG Asia Mater. 12, 1–16 (2020).
Naresh, K. & Utpal, B. Silk fibroin in tissue engineering. Adv. Healthc. Mater. 1, 393–412 (2012).
Kim, S. H. et al. 4D-bioprinted silk hydrogels for tissue engineering. Biomaterials 260, 120281 (2020).
Ajiteru, O. et al. A 3D printable electroconductive biocomposite bioink based on silk fibroin-conjugated graphene oxide. Nano Lett. 20, 6873–6883 (2020).
Van Den Bulcke, A. I. et al. Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules 1, 31–38 (2000).
Yue, K. et al. Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels. Biomaterials 73, 254–271 (2015).
Li, X., Zhang, J., Kawazoe, N. & Chen, G. Fabrication of highly crosslinked gelatin hydrogel and its influence on chondrocyte proliferation and phenotype. Polymers 9, 309 (2017).
Kim, H. et al. Effect of silk fibroin molecular weight on physical property of silk hydrogel. Polymer 90, 26–33 (2016).
Ozbas, B., Kretsinger, J., Rajagopal, K., Schneider, J. P. & Pochan, D. J. Salt-triggered peptide folding and consequent self-assembly into hydrogels with tunable modulus. Macromolecules 37, 7331–7337 (2004).
Ladner-Keay, C. L., Griffith, B. J. & Wishart, D. S. Shaking alone induces de novo conversion of recombinant prion proteins to β-sheet rich oligomers and fibrils. PloS One 9, e98753 (2014).
Kim, U.-J. et al. Structure and properties of silk hydrogels. Biomacromolecules 5, 786–792 (2004).
Xu, H., Casillas, J., Krishnamoorthy, S. & Xu, C. Effects of Irgacure 2959 and lithium phenyl-2, 4, 6-trimethylbenzoylphosphinate on cell viability, physical properties, and microstructure in 3D bioprinting of vascular-like constructs. Biomed. Mater. 15, 055021 (2020).
Fairbanks, B. D., Schwartz, M. P., Bowman, C. N. & Anseth, K. S. Photoinitiated polymerization of PEG-diacrylate with lithium phenyl-2, 4, 6-trimethylbenzoylphosphinate: polymerization rate and cytocompatibility. Biomaterials 30, 6702–6707 (2009).
Xu, L., Sheybani, N., Yeudall, W. A. & Yang, H. The effect of photoinitiators on intracellular AKT signaling pathway in tissue engineering application. Biomater. Sci. 3, 250–255 (2015).
Wray, L. S. et al. Effect of processing on silk‐based biomaterials: reproducibility and biocompatibility. J. Biomed. Mater. Res. B Appl. Biomater. 99, 89–101 (2011).
Kim, J. et al. Comparison of methods for the repair of acute tympanic membrane perforations: silk patch vs. paper patch. Wound Repair Regen. 18, 132–138 (2010).
Zhang, F. et al. Silk dissolution and regeneration at the nanofibril scale. J. Mater. Chem. B 2, 3879–3885 (2014).
Gupta, D., Agrawal, A., Chaudhary, H., Gulrajani, M. & Gupta, C. Cleaner process for extraction of sericin using infrared. J. Clean. Prod. 52, 488–494 (2013).
Dou, H. & Zuo, B. Effect of sodium carbonate concentrations on the degumming and regeneration process of silk fibroin. J. Text. Inst. 106, 311–319 (2015).
You, R., Zhang, Y., Liu, Y., Liu, G. & Li, M. The degradation behavior of silk fibroin derived from different ionic liquid solvents. Natural Science 5, 10–19 (2013).
Murphy, A. R. & Kaplan, D. L. Biomedical applications of chemically-modified silk fibroin. J. Mater. Chem. 19, 6443–6450 (2009).
Mondal, M., Trivedy, K. & Nirmal, K. S. The silk proteins, sericin and fibroin in silkworm, Bombyx mori Linn., a review. Caspian. J. Environ. Sci. 5, 63–76 (2007).
Nichol, J. W. et al. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 31, 5536–5544 (2010).
Yadav, D. & Gaikwad, A. Comparison and testing of tensile strength for low & medium carbon steel. Int. J. Mech. Eng. 4, 1–8 (2015).
Fergg, F., Keil, F. & Quader, H. Investigations of the microscopic structure of poly (vinyl alcohol) hydrogels by confocal laser scanning microscopy. Colloid Polym. Sci. 279, 61–67 (2001).
Lee, J. S. et al. 3D-printable photocurable bioink for cartilage regeneration of tonsil-derived mesenchymal stem cells. Addit. Manuf. 33, 101136 (2020).
Steehler, M. K., Hesham, H. N., Wycherly, B. J., Burke, K. M. & Malekzadeh, S. Induction of tracheal stenosis in a rabbit model—endoscopic versus open technique. Laryngoscope 121, 509–514 (2011).
Den Hondt, M., Vanaudenaerde, B. M., Delaere, P. & Vranckx, J. J. Twenty years of experience with the rabbit model, a versatile model for tracheal transplantation research. Plast. Aesthetic Res. 3, 223–230 (2016).

3D bioprinted silk fibroin hydrogels for tissue engineering

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