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Silk Fibroin-Based 3D Printing Strategies for Biomedical Applications

Xiaoxue Gu , Jing Yu , Mingying Yang , Yajun Shuai

Progress in Chemistry ›› 2022, Vol. 34 ›› Issue (6) : 1359 -1368.

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Progress in Chemistry ›› 2022, Vol. 34 ›› Issue (6) : 1359-1368 DOI: 10.7536/PC210633
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Silk Fibroin-Based 3D Printing Strategies for Biomedical Applications
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Abstract

Additive manufacturing, also known as three-dimensional (3D) printing, drives comprehensive innovations and upgrades in manufacturing, engineering, medicine, and other fields. 3D printing technology has made great progress in the biomedicine field in the past decade due to its ability to customize the complex 3D microstructures of organisms and construct biomimetic functional living tissues or artificial organs. In addition, silk fibroin (SF) is a natural organic polymer with abundant sources, biodegradable, excellent mechanical properties, and good cytocompatibility, which provides a promising choice for the design of 3D-printing inks. However, as a structural protein, single-component SF has limited physiological functions, and poor stability after printing, which limits the further development of SF in 3D printing and biomedical fields. For these reasons, researchers combined advanced 3D printing technologies with chemical modification methods to make the modified SF easy to be used for 3D printing and develop into a valuable biomaterial. Here, this article reviews the structural characteristics of SF, chemical modification strategies of SF, preparation strategies of printing inks and the latest application progress of 3D printed SF materials in the biomedical field. Meanwhile, we also look forward to the future development trend of 3D printed SF biomaterials, which provides a useful guideline for its application in a wider field.

Contents

1 Introduction

2 The structures and characteristics of SF

3 Preparation strategies of bio-inks

3.1 Compounding with polymers

3.2 Compounding with inorganics

3.3 Self cross-linking

3.4 Chemical modification

4 3D printing technologies

4.1 Inkjet

4.2 Extrusion

4.3 Photo-curing

5 Applications in the field of biomedical

5.1 Blood vessel regeneration

5.2 Cartilage repair

5.3 Bone repair

5.4 Skin healing

6 Conclusions and outlook

Graphical abstract

Keywords

3D printing / silk fibroin / bio-ink / biomaterial

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Xiaoxue Gu, Jing Yu, Mingying Yang, Yajun Shuai. Silk Fibroin-Based 3D Printing Strategies for Biomedical Applications. Progress in Chemistry, 2022, 34(6): 1359-1368 DOI:10.7536/PC210633

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1 Introduction

Silk fiber is not only a kind of high-grade textile raw material, but also a valuable natural organic polymer resource. It includes mulberry silk (also known as domestic silk) and non-mulberry silk (such as tussah silk, castor silk, natural silk, etc.)[1⇓⇓~4]. A single silk fiber is composed of two silk fibroin single fibers wrapped by sericin. After the sericin on the surface of silk fiber is removed by degumming process, the regenerated silk fibroin (SF) aqueous solution can be obtained by dissolution[5]. Using regenerated silk fibroin aqueous solution as raw material, SF biomaterials with various forms and scales can be prepared by traditional processing techniques and means such as freeze-drying, phase separation, electrospinning, gas foaming, solvent pouring, etc., which can be used for the repair of damaged tissues and organs and the application of flexible sensors[6⇓⇓⇓⇓⇓~12]. Although traditional biomaterials preparation methods can prepare porous scaffolds with regular shapes, the lack of porosity, porous interconnection and complex and fine micro-nano structures required for tissue cell migration and differentiation limits the further application of these biomaterials in the biomedical field[13].
3D printing technology can design and manufacture complex and precise microstructures and geometric shapes according to actual needs to promote the regeneration of damaged tissues and organs in vivo, so it has advantages that traditional scaffold preparation methods do not have, and plays an important role in the biomedical field in recent years[14⇓⇓⇓⇓~19]. SF has been chosen by more and more researchers as the raw material for 3D printing due to its abundant sources, variety, processing and chemical modification, and has been widely used in the biomedical field[20⇓⇓⇓~24].
In the past five years, there have been increasing reports on the research and application of 3D printing SF, but there are few related review articles[18]. Therefore, this review systematically reviews the latest research progress in this field, summarizes the experience and rules, and looks forward to the new functions and uses of silk with ancient history through 3D printing technology.

2 Structure and Characteristics of Silk Fibroin

The most studied silk fiber of Bombyx mori is composed of about 70% SF, 25% sericin, and about 5% other substances. SF is composed of three subunits, heavy chain, light chain and glycoprotein P25, which are bound by disulfide bonds and hydrophobic bonds[25,26]. Its secondary structure is mainly composed of two conformations: random coil and β-sheet. Biomaterials with different morphologies and properties can be prepared by regulating the composition of secondary structures and the proportion of each structure[27,28].
Because the peptide chain of SF contains about 1/4 of polar amino acids, it is easy to introduce bioactive groups to endow SF with specific functions by chemical or physical methods, thus improving the structural stability and biofunctionality of 3D printing SF materials[29⇓~31].

3 Bioink preparation strategy

The design of bioink is a crucial step in the 3D printing process, in which several important parameters, including the shear thinning characteristics of the ink solution, cell compatibility, swelling ratio, surface tension, and gel dynamics, are variables that need to be considered[32,33]. A reasonable choice must be made based on the specific printing and application requirements. Like many biological macromolecules, the regenerated SF solution does not satisfy these properties in its natural state and needs to be further modified and optimized before it can meet the demand for printability (Table 1).

3.1 Polymer composite method

Based on the physical and chemical properties of SF, composite 3D printing solution can be prepared by mixing SF with other polymers such as gelatin, alginate, chitosan, polyethylene glycol, cellulose, etc[41]. Some scholars even reported that silkworm SF, eri-silkworm SF and gelatin were compounded to prepare ternary printing solution[22]. By optimizing the basic parameters of the composite printing solution, the shape fidelity, printability, mechanical properties and cell survival rate of 3D printing materials can be changed[42⇓⇓⇓⇓⇓⇓~49].
Rodriguez et al. Mixed glycerol in SF solution at a fixed ratio of 3:1, then mixed SF/glycerol solution with gelatin solution at a ratio of 2:1, and then vortexed to obtain SF/gelatin composite printing solution[20]. Because the insoluble structure can be quickly generated after the SF and the glycerol are mixed, and the gel-sol phase transition process of the gelatin is controlled by the temperature, the SF/glycerol/gelatin composite printing solution can be used for 3D printing without adding other toxic crosslinking reagents.
In order to prove the possibility of preparing composite ink between SF and synthetic polymer, Zheng et al. Mixed SF with molecular weight greater than 200 kDa with polyethylene glycol and incubated at 37 ℃ to a pre-gel state to obtain a composite printing solution[50]. The printing results show that the high concentration range of SF gel (7.5%, w/V) can show better shape fidelity during printing compared with the low concentration of SF gel (2.5%, w/V).

3.2 Inorganic composite method

In recent years, mesoporous bioactive glass (MBG) has been widely used as a good drug carrier and an ideal bone repair material. Du et al. Prepared an MBG/SF printing precursor solution with a concentration of 30 wt% SF as the organic phase and MBG as the inorganic phase according to the mass ratio of the solution (MBG/SF) of 80% ∶ 20%[51]. The scaffolds printed with the precursor solution have superior compressive strength (about 20 MPa), good biocompatibility and the ability to promote bone formation. In addition, reduced graphene oxide (rGO) has unique physical and chemical properties, which has attracted much attention in the preparation of conductive biocomposites. Ajiteru et al. Prepared a conductive 3D printing premix solution by modifying the methacrylated SF solution with carbodiimide reagent and then mixing it with the ultrasonically dispersed rGO solution[52]. The scaffold material based on the premix has unique electrical and biological properties, and can induce neuroblast to differentiate into neurons without adding additional cell differentiation inducing substances, thereby having the potential function of promoting nerve tissue regeneration.

3.3 Silk fibroin self-crosslinking method

At room temperature, a certain concentration of SF solution can self-gel without the addition of any ions and chemical reagents, but the process is relatively slow (usually the time span is between a week and half a year). SF can be rapidly transformed from solution state to sol state by external environmental stimulation, such as mechanical stirring, ultrasound, heat treatment, low pH and alcohol solution treatment, so as to prepare SF precursor liquid for 3D printing. As early as 2008, Lewis's research group printed SF precursor solution with a mass fraction of 28% -30% into a grid structure based on extrusion printing, and promoted the transformation of SF from a random coil state to a β-sheet structure by soaking in a methanol-rich coagulation tank, thus obtaining a structurally stable SF printing scaffold[39].
However, the gelation process using the external environment to stimulate SF is not conducive to the viability of cells encapsulated in the precursor solution. By adjusting the molecular weight of SF solution and changing the condensed structure in the microsolvent, the rheological properties of pure SF printing solution can be improved, making it suitable for bio-3D printing. Tao et al. Prepared SF precursor solutions with a final concentration of 3 wt% and a molecular weight between 90 and 350 kDa[33]. The SF solution was then printed using an inkjet printer to form stable droplets with a suitable dynamic viscosity (3 mPa · s) and surface tension (0.046 N/m) for rapid solidification and molding. The printing method can achieve a resolution of 20 μm and promote the proliferation and osteogenic differentiation of coated human bone marrow mesenchymal stem cells (hMSCs).

3.4 Chemical modification method

Because there are many kinds of active amino acids on the SF peptide chain, including serine, tyrosine, lysine, glutamic acid, etc., the chemical modification between SF peptide chains is easy to achieve, such as grafting reaction, crosslinking reaction, functional group reaction, etc., which is conducive to the preparation of printing precursors[53⇓⇓~56]. Zhang Yaopeng's team has developed a precursor solution for 3D printing, which includes oxidized bacterial cellulose nanofibers (OBC) and SF[36]. SF was cross-linked by horseradish peroxidase (HRP)/H2O2 to form a scaffold, and 7 wt% OBC increased the viscosity of the precursor during printing and further improved the shape fidelity of the scaffold. In addition, cell experiments showed that lung epithelial stem cells (LESCs) seeded on the SF-OBC printed scaffold could maintain rapid proliferation for at least one week, making the printed scaffold promising for lung tissue engineering (Fig. 1).
Kim et al. Added glycidyl methacrylate (GMA) to SF solution for sufficient reaction to prepare GMA-modified SF ink (Sil-MA)[40]. SF modified by GMA introduces photocrosslinking sites, which can be cured layer by layer by ultraviolet irradiation in a photocuring 3D printer to construct a complex artificial organ (Fig. 2).
After that, the research group further tried to use this type of scaffold to repair the rabbit tracheal defect model, which can effectively improve the proliferation and migration of cells inside the printed scaffold, and is expected to be used for the regeneration and repair of human damaged organs and tissues in the future[57].
Because SF has about 5% tyrosine residues, phenolic photocrosslinking between SF molecules can occur. Riboflavin can produce reactive oxygen radicals (ROS), mainly singlet oxygen, by visible light irradiation, and then induce chemical cross-linking between SF molecules to form dityrosine bonds. Using this principle, Shin et al. Mixed SF solution with 0. 5 mmol/L riboflavin solution to prepare a precursor solution for 3D printing[58]. The SF hydrogel microneedles obtained by 3D printing have high mechanical strength, and the microneedle structure will not be seriously damaged after a compressive stress of about 300 mN is applied. At that same time, preparation of SF precursor solution by combination of transition metal complexes, ruthenium (Ru) and persulfate compound has been investigated[59]. During photoactivation, photolysis of Ru2+ produces excited Ru3+, which oxidizes the tyrosine group and then cross-links SF by forming a dityrosine bond with the neighboring tyrosine. Cui et al. Used this visible-light-mediated photoredox system to crosslink SF molecules, which can produce a rapid photocrosslinking reaction (< 1 min) between SF molecules[60]. Compared with the enzymatically crosslinked SF hydrogel, the photocrosslinked SF hydrogel showed more stable mechanical properties, and its compressive modulus remained stable within five weeks (fig. 3), which played a positive role in maintaining the homeostasis of cells.

4 3D printing technology

3D printed SF scaffolds have been widely used in the construction of tissue and organ prototypes, which not only lays the foundation for the ambitious goal of repair and replacement of human injured organs, but also can be used as an in vitro model service for drug screening and other fields. At present, there are many 3D printing technologies that can be applied to silk fibroin, mainly including inkjet printing, extrusion printing and light curing printing (Fig. 4). Different types of printers have different printing resolution, printing speed and cell printing density, and the appropriate printer type should be selected according to the specific application (Table 2).

4.1 Inkjet printing

Inkjet printing is a technique for liquid phase material deposition. This process is essentially a technique for accurately coating a substrate with a large number of tiny ink droplets (usually only a few picoliters) ejected from a nozzle[65⇓~67]. As early as 2006, Kaplan's team first used inkjet printing technology to print 0.6% w/w SF solution into parallel line structure on transparent vinyl plastic[68]. One week after hMSCs were seeded on the printed parallel line pattern, hMSCs were able to spread and differentiate into osteoblasts along the printed SF parallel lines. After 4 weeks of culture, cells on adjacent parallel lines with a line spacing of less than 1.25 mm were bridged. This result is the first step for inkjet printing SF materials to regulate cell growth behavior.

4.2 Extrusion printing

Extrusion printing is a common bioprinting method. The printing process comprises the following steps of: firstly, injecting the bio-ink or the printing stock solution into a reservoir connected with a nozzle; and then, at a certain temperature, extruding the ink layer by layer from a micro-nozzle of the printer and curing and forming the ink on a printing platform. Similar to inkjet printing, the printing dope must be cured quickly and controllably to produce a mechanically stable printing material[69,70].
Lewis's group was the first to try to print SF biomaterials with an extrusion printer[39]. The team successfully printed SF solutions with concentrations ranging from 28% to 30% into square lattices and circular mesh scaffolds. It was found that when the shear rate was increased above 100 s-1, the solution showed obvious shear thickening behavior due to the transition of SF solution to β-sheet, which led to the blockage of the micro-nozzle during printing. In order to avoid shear thickening in the printing process, many research groups have made efforts[71,72]. Ghosh's group added gelatin to SF solution to prepare SF/gelatin precursor solution, which showed shear thinning effect in a certain concentration range, so it was easy to extrude from the nozzle[73]. This phenomenon may be caused by the hydrophobic and electrostatic interaction between the two protein macromolecular chains.
Shape fidelity and adjustable mechanical strength are important factors to be considered in extrusion 3D printing. This means that the printed product needs to maintain its shape stability after a period of cell culture, and the implanted hydrogel scaffold can only meet the needs of natural tissue repair if it reaches a certain magnitude of stiffness. For example, for mammalian native articular cartilage explants, the equilibrium modulus and dynamic stiffness are 0.27 and 0.41 MPa, respectively[74,75]. For skeletal muscle implants, typical values of stress and strain are approximately 100 kPa and 20%, respectively[76]. Based on this, Jose et al. Used gelatin as a filler to add to the polyol/SF printing precursor solution formulation, and printed SF-based scaffolds with a modulus of 15.2 ± 2.5 kPa[77]. Rodriguez et al. Increased the elastic modulus of the composite scaffold from 50 Pa to 1000 Pa by treating the printed SF/gelatin scaffold with glycerol[20]. However, the mechanical properties of this type of stent still have much room for improvement. In order to overcome the above problems, Zhang Yaopeng's team significantly enhanced the shape fidelity and mechanical properties of the composite scaffold based on extrusion printing by adding 0. 7 wt% bacterial cellulose nanofibers (BCNFs) to SF/gelatin composite bioink[37]. The experimental results show that the elastic modulus of the scaffold based on BCNFs reaches 186. 5 kPa, and the scaffold has high shape fidelity.

4.3 Photocuring printing

Photo-curing printing is a method of using the light source in the printer to cure the photosensitive resin and accumulate it into a three-dimensional model point by point or layer by layer[78⇓~80]. Optical curing printers are mainly divided into stereolithography (SLA), digital light processing (DLP) and selective area curing (LCD). The principle of SLA printing imaging is to use laser as a light source for laser spot scanning imaging, and then make ink printing. DLP is printed by ultraviolet projection of the cross section of the product and curing the liquid photosensitive material layer by layer[40,81]. DLP printing has higher printing resolution and printing speed, which greatly improves the integrity and mechanical properties of the printing structure, and is widely used in SF-based 3D printing technology. The principle of LCD printing is similar to that of DLP, which is surface molding. The difference is that DLP uses a digital projector to project the light source, while LCD uses an ordinary LCD screen to project.
Pure SF solution cannot be directly used for DLP printing because it cannot be photopolymerized[82]. In order to solve this problem, Kim et al. Modified SF with GMA to introduce photosensitive groups, so that SF can be used for DLP printing, and proved that the printing process has no damage to cells, and the printed scaffold structure has good biocompatibility[40].
Currently, a variety of acrylate-modified polymer materials have been developed for SLA printing[83⇓~85]. Because the printing resolution of SLA printer depends on the penetration depth of light through ink, however, acrylate modified polymer materials are transparent, and light has strong penetration in transparent solution, resulting in uncontrollable printing resolution. To this end, Shin et al. Combined SF with melanin nanoparticles (SFM) as a transparency modifier for four-arm polyethylene glycol-acrylate (PEG4A) solution[86]. By adding SFM to the PEG4A solution, the beam can be confined to the set area, which effectively reduces the transparency of the solution and improves the printing resolution. In addition, the elastic modulus of the PEG4A/SFM composite hydrogel after printing is about 2.5 times higher than that of the PEG4A hydrogel without SFM.

5 Application in the biomedical field

5.1 Revascularization

The vascular system within a tissue or organ is essential in transporting oxygen and nutrients, substance metabolism[87]. However, the artificial blood vessel prepared by traditional methods has some shortcomings, such as irregular shape, easy to form thrombus after implantation, which limits its clinical application. Kim et al. Successfully used modified SF ink to 3D print tubular vascular structures, and showed excellent mechanical and rheological properties, which provided a variety of possibilities for later in vitro culture of highly vascularized organs[40].

5.2 Cartilage repair

Cartilage is a kind of non-vascular connective tissue. Because of its poor mitotic ability, it is difficult to cure cartilage injury[88]. Traditional cartilage repair methods still have a big gap in simulating the fine structure of natural cartilage tissue, especially the micro-nano ordered structure. Using 3D printing technology, extracellular matrix-like scaffolds with micron-sized and highly complex structures can be prepared[89]. Shi et al. Used 3D printing technology to prepare SF/gelatin scaffolds for rabbit cartilage repair. The ingenious combination of SF and gelatin greatly balanced the mechanical properties and degradation rate of the scaffolds, which could match the growth rate of cartilage tissue, thus effectively promoting the repair of rabbit knee cartilage[21]. Xiao et al. Prepared an interpenetrating polymer network (IPN) hydrogel loaded with MC3T3-E1 preosteoblasts by continuous ultrasonic and photocrosslinking using methacrylate gelatin and SF for cartilage tissue repair[90]. The cells had a high survival rate and good proliferation status after the third day of culture. The hydrogel is stable in biological function and biomechanics, and can regulate the growth of encapsulated cells by adjusting the concentration of GelMA.

5.3 Bone repair

Congenital defects, neoplastic diseases, and trauma can cause severe skeletal defects[91]. The use of 3D printing-based scaffolds provides an effective solution to the above problems. Kaplan's team patterned the SF/hydroxyapatite scaffold into a 3D lattice-like structure by direct write printing, which is composed of interconnected SF/hydroxyapatite with interconnected pore channels and gradient networks[92]. In vitro experiments showed that hMSCs seeded on scaffolds with pore sizes ranging from 200 μm to 750 μm could spread over the scaffolds after 6 weeks of culture, and type I collagen, a typical marker of bone tissue, could be layered on all scaffolds with different pore sizes, indicating that the scaffolds were expected to be used for the repair of defective bone tissue.

5.4 Skin repair

The skin is the largest organ of the human body and primarily serves as a protective barrier between the body and the external environment[93⇓~95]. In daily life, the skin is inevitably in direct contact with harmful microorganisms and is vulnerable to mechanical, thermal, and chemical damage. Xiong et al. Prepared a sulfonated gelatin/SF composite scaffold by 3D printing, and combined basic fibroblast growth factor 2 (FGF-2) on the scaffold[96]. Histological results showed that this SF composite scaffold combined with FGF-2 could support the formation of granulation tissue and significantly promote the regeneration of rat skin tissue (Fig. 5).

6 Summary and Prospect

In this paper, the basic properties of SF are described, the chemical modification of SF, the preparation of printing precursor solution and the 3D printing technology are discussed, and the specific applications of 3D printing SF biomaterials in the biomedical field are introduced.
Although silk has been used as a textile fiber for more than 5000 years, its application in 3D bioprinting has just begun, and it still needs concentrated efforts from many aspects to realize the clinical application of this technology. On the one hand, the existing SF-based bioinks are limited to explore in a limited range, while most human organs such as heart, kidney and liver are composed of different types of cells and tissues.Therefore, 3D printing materials composed of a single cell type and a single raw material component cannot simulate the actual situation in vivo, and chemical modification technology and tissue engineering technology are needed to further improve the simulation of SF-based living cell printing scaffolds, from similarity in form to similarity in spirit. On the other hand, the stability, functionality and accuracy of 3D printing SF materials need to be further improved. Although 3D printing technology has shown great advantages in precision and personalized treatment, it has not yet reached mature application in the biomedical field due to the development of equipment and materials. However, with the deepening of researchers' understanding of the physical and chemical properties of SF, the continuous development of printing materials, the continuous updating of printing equipment, and the continuous development of new printing strategies such as support bath suspension printing, 4D printing, heterostructure printing, and gradient material printing, the application of SF-based 3D printing technology in the biomedical field will become more and more mature and diversified[97].

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Funding

National Natural Science Foundation of China(31800807)

Zhejiang Provincial Science and Technology Plans(LY22E030004)

Fundamental Research Funds for the Central Universities(2020QNA6028)

State of Sericulture Industry Technology System(CARS-18-ZJ0501)

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