Enzyme biotechnology for medical textiles

Enzyme biotechnology for medical textiles

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Ivaylo Stefanov, Arnau Bassegoda, Tzanko Tzanov Department of Chemical Engineering, Universitat Polit
ecnica de Catalunya, Terrassa, Spain

7.1

Introduction

In the past, natural-based textile bandages were traditionally used for covering and treatment of cutaneous injuries with the only function to protect the wound from external damage. Nowadays, simple bandages are still on market as important part of wound care; however, the intrinsic flexibility, robustness, and strength of textiles have rendered them irreplaceable in modern medical procedures, expanding the term “biomedical textiles” beyond simple inert protective textiles. Fiber components can be found in a variety of structures ranging from nonwoven bandages for wound healing (Rajendran, 2009; Van Langenhove, 2015) to more complex hollow fiber membranes (HFMs) for high-performance life-saving devices, such as artificial lungs (Ye et al., 2015) and kidneys (An et al., 2017). The application of textiles covers broad medical areas, including surgery, where textile-based sutures for stapling of surgical wounds are widely used (Catanzano et al., 2014; Annabi et al., 2014), and tissue engineering, where textiles mimic tissues and support regeneration of organs, such as cartilage (Moutos et al., 2007; Chen et al., 2017a), ligament (Edwardsl et al., 2006), vasculatures (Hasan et al., 2014; Zhao et al., 2013), bones (Nagarajan et al., 2017; Chen et al., 2017b), heart (S¸enel Ayaz et al., 2014), and skin (Chaudhari et al., 2016). On the other hand, textile platforms for microfluidic bioanalytical devices in point-of-care diagnostics are developed, featuring high tensile strength and flexibility, controllable rates for fluid mixing, low precise control requirements of sample volumes, and reduced environmental impact (Nilghaz et al., 2013; Bagherbaigi et al., 2014). These advances show how the medical application of textiles is limited solely by the textiles’ versatility. The development of textiles with incorporated biofunctionalities has potential to not only improve their function but also expand their application to new medical fields. For instance, nonwoven bandages with antimicrobial activities would provide efficient wound treatment, while the design of enzymeresponsive textiles might have potential also in gene therapy and biosensing. The development of biofunctional textiles is related to the incorporation of biomolecules, thus, demanding the application of mild processing conditions, which are not usually applied in traditional textile manufacturing. Novel bioactive textile structures stem from a mandatory inter- and multidisciplinary interaction, merging engineering sciences and biotechnological advances. Biotechnology for the development of biomedical textiles can be considered in terms of (1) enzymatically assisted modification of the fibers, (2) introduction of Advances in Textile Biotechnology. https://doi.org/10.1016/B978-0-08-102632-8.00007-4 Copyright © 2019 Elsevier Ltd. All rights reserved.

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new functionalities through immobilization of enzymes on textiles, and (3) the development of bioresponsive textile materials, which change their chemical or physicochemical properties on enzymatic activity in biological environment. The contents of this chapter are organized according to these three biotechnical applications. Challenges and benefits that researchers face when combining biotechnology with textile technologies for development of biomedical textiles are outlined. The choice of the textile material for the desired biofunctionalization, the potential and limitations of enzymes for textile modification and/or incorporation of biomolecules in textiles, and the combination of these biotechnical approaches with different additive technologies such as electrospinning, electrospraying, ultrasonication, or layer-by-layer (LbL) deposition are overviewed.

7.2

Enzymatic functionalization of biomedical textiles

Textiles can be substrates for enzymatic functionalization or serve as supports for immobilization of bioactive molecules to impart novel properties. The presence of numerous functional groups in the chemical structure of natural and synthetic fibers offers a variety of grafting options for the bioactive agents. For instance, fibers of synthetic origin, such as poly(acrylonitrile) (PAN) or poly(ethylene terephthalate) (PET), are rich in nitrile and ester groups, which on reduction or hydrolysis are converted into amino or carboxylic groups for grafting of bioactives (Guebitz and Cavaco-Paulo, 2008). Natural fibers, such as wool and cotton, contain amino, thiol, phenolic, or hydroxyl groups that can be used to bind functional molecules through amide (Cortez et al., 2005) and disulfide bonds (Fernandes et al., 2011), Michael addition reactions and Schiff base formation. Nevertheless, most textile polymers need surface functionalization before attachment of the bioactive compound because of chemical inertness of the fiber polymer or engagement of its functional groups in strong macromolecular interactions leading to high degree of crystallinity. Surface preactivation is conventionally achieved chemically by coating with, e.g., silane monolayers or physically by ionized gas (plasma) treatments and UV irradiation (Goddard and Hotchkiss, 2007). These techniques, however, could also change the bulk properties of the textile substrate, require multistep reactions decreasing the final reproducibility, and lead to accumulation of hazardous chemicals (John and Anandjiwala, 2012). Alternatively, enzymes represent an efficient tool for textile functionalization. The enzyme chemoselectivity can be exploited to target specific chemical groups in fiber structure. Two main strategies for enzymatic functionalization of textiles with bioactives may be adopted: (1) enzymatic generation of reactive functional groups on the fiber, which serve as anchoring points for immobilization of the bioactive agent (Fig. 7.1(a)) or (2) enzymatic activation of a biomolecule of interest to react with the textile functional groups (Fig. 7.1(b)). Both strategies can be combined; for instance, enzymes can react and activate simultaneously the molecule of interest and the textile polymer. From an environmental point of view, employment of enzymes in textile processing usually leads to reduced energy cost, water consumption, and amount of waste (Madhu and Chakraborty, 2017). Enzymatically assisted functionalization offers

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(a)

(b)

Enzyme Bioactive molecule (BM) Enzymatically activated BM Textile polymer functional group (TPFG) Enzymatically modified TPFG Textile

Figure 7.1 Strategies for enzymatically assisted functionalization of textiles for biomedical applications. (a) Enzymatic generation of reactive functional groups on the fiber, which subsequently undergo chemical reaction with the bioactive. (b) The enzyme acts on the molecule of interest, which on activation undergoes chemical reaction with the polymer functional groups.

mild processing conditions in terms of temperature and pH and minimizes the exposure of textiles to chemical reagents and organic solvents. This avoids timeconsuming washing steps and reduces costs through water and energy saving, which is a major challenge in textile industry (Shahid et al., 2016). Furthermore, the use of enzymes allows the manufacture of textiles free of chemicals, an added value particularly relevant for biomedical applications minimizing possible adverse reactions. Despite the great potential of enzymes as tools for textile engineering, their application is still limited. The main hurdle of enzymatically assisted textile functionalization is the nonnatural solid form of the substrate, contrasting with the easily accessible soluble one in the living organisms’ microenvironment, causing heterogeneous conditions where the accessibility of the enzyme to the substrate is restricted and often diffusion-controlled (Warmoeskerken and Boewhuis, 2010). Nevertheless, when aiming to incorporate biofunctionalities into textiles for biomedical purposes, enzymes represent the optimum tool. Their use allows the textile modification to achieve the desired biofunctionality while avoiding the use of harsh chemical/conditions, thus fulfilling with the safety conditions demanded for the medical application of a material. In this section, we review how the use of enzymes has allowed different textile modifications incorporating a variety of elements, from small molecules to polymers or metal nanoparticles (NPs).

7.2.1

Enzymatic fiber modification for incorporation of bioactives

Oxidoreductases are a class of enzymes capable of oxidizing a wide range of substrates, in particular monophenols and polyphenols (Abdel-Mohsen et al., 2014;

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Kudanga et al., 2017). This class of enzymes can be used to oxidize phenolic molecules of interest to highly reactive quinone species, which can easily react with nucleophiles such as amino and thiol groups, present in the fiber structure. Jus et al. described an enzymatic method for grafting natural antioxidant phenolics, such as chlorogenic and caffeic acids on wool fibers using the oxidative enzyme tyrosinase (EC 1.14.18.1). Tyrosinase catalyzes the orthohydroxylation of monophenols and the subsequent oxidation of the diphenol to the corresponding quinone. The enzyme oxidized both the tyrosine residues of wool proteins and the phenolic molecules leading to cross-coupling reactions or Michael-additions of nucleophilic amino and sulfhydryl groups from lysine and cysteine residues present in wool (Jus et al., 2008). The aforementioned reaction pattern has been used to functionalize silk fibroin with various bioactive molecules to achieve improvement of its properties for potential biomedical applications. Following this rationale, the antibacterial biopolymer chitosan was enzymatically grafted onto silk fibroin fabric, where the oxidized tyrosine residues in silk reacted with the amino groups in chitosan. The chitosan-modified silk fabric revealed durable antibacterial effect against Staphylococcus aureus (Yuan et al., 2014). In another work, antibacterial properties of silk fabric were achieved by grafting the protein lactoferrin through tyrosinase-catalyzed oxidation of tyrosyl residues in silk fibroin to quinones, which further reacted with the lactoferrin amino groups. The fabrics pretreated with tyrosinase showed greater antibacterial activity against both Grampositive and Gram-negative strains compared with the fabrics treated with lactoferrin alone (Wang et al., 2014). Tyrosinase-assisted grafting of ε-polylysine (ε-PLL) was explored to enhance the antibacterial performance of silk fibroin. Before tyrosinase treatment, the silk fibroin membrane was pretreated with 2,4,6-trinitrobenzene sulfonic acid to prevent the protein from selfecross-linking and to promote the grafting of ε-PLL. The functionalized silk fibroin revealed improved antibacterial activity against Gram-positive bacteria (Wang et al., 2016a). Wang et al. suggested a way to improve the enzymatic reactivity of silk fibroin membrane by grafting tyrosine-containing peptide through 1-Ethyl-3-[3-dimethyl aminopropyl]carbodiimide hydrochloride (EDC) chemistry. Then, the tyrosinase oxidized tyrosyl residues in the peptide-functionalized fibroin reacted through Schiff base or Michael addition reaction with the amino groups of ε-PLL (Wang et al., 2016b). The method was further upgraded by replacement of the synthetic crosslinker EDC with the naturally occurring genipin (Zhu et al., 2017). Hong and co-authors fabricated hybrid silk fibroin/elastin bioscaffold through tyrosinase-assisted oxidation of silk fibroin tyrosyl residues and their subsequent reaction with elastin nucleophilic groups. The hybrid membranes revealed high biocompatibility of NIH/3T3 cells, envisaging their potential for biomedical applications (Hong et al., 2016). Silk fibroins have been utilized as a growth substrate for hydroxyapatite (HAp) deposition. For this purpose, acrylic acid was graft copolymerized on the silk fibroin chains by using hydrogen peroxide/horseradish peroxidase (HRP) catalytic system to obtain grafted copolymer silk fibroinegrafted polyacrilic acid (SF-g-PAA).

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Thereafter, composite membranes SF-g-PAA/HAp were prepared via in situ biomimetic mineralization. The prepared composite membranes promoted the adhesion and proliferation of osteoblast cells, rendering them valuable products for bone tissue engineering (Zhou et al., 2017a). Oxidative enzymes, such as HRP, can be used for improving the mechanical properties of silk fibers and thus expanding the field for biomedical applications. The incubation of the model compound of silk fibroin tyrosine residuesdp-hydroxyphenyl acetamidedwith the HRP/hydrogen peroxide system led to its polymerization. The molecular weight of silk fibroin noticeably increased, which evidenced the compound grafting achieved using the enzymatic system. The mechanical and thermal properties of silk fibroin were significantly improved and the biocompatibility tests showed high cell viability of NIH/3T3 cells, envisaging their potential biomedical application (Zhou et al., 2017b). Silk fibroins can be used as a graft material to increase the biocompatibility of materials with relatively high toxicity. In this sense, silk fibroin was grafted on bacterial cellulose membrane through laccase and 2,20 ,6,60 -tetramethylpiperidine-N-oxyl (TEMPO) oxidizing system. The obtained membranes exhibited improved biocompatibility, compared with the untreated cellulose membrane (Zhou et al., 2017c). The antioxidant ability of silk fibroin was enhanced by immobilization of catechin through using tyrosinase as an oxidizing agent. The oxidized catechin reacted with the amino groups of lysyl residues to form a novel membrane, which despite the possible reduction in the catechin antioxidant capability after the enzyme oxidative action did not reveal any significant differences with the membrane treated with catechin alone (Qi et al., 2016). Laccase-assisted functionalization of silk fibroin with chitooligosaccharides (COS) resulted in silk fibroin membranes with enhanced antibacterial and antioxidant properties, paired to satisfactory biocompatibility. This functionalization was achieved by laccase oxidation of the tyrosyl residues in silk fibroin into the highly reactive quinones, which subsequently reacted with the amino groups of COS (Zhou et al., 2018). Besides activating functional groups, enzymes are also able to generate new ones in the chemical structure of the textile material. With the aim to produce fabrics that decrease bleeding time, Akkaya et al. grafted the serine protease thrombin (EC 3.4.21.5) onto PET and PAN fabrics. Thrombin is an enzyme, which contributes for clot formation during coagulation converting fibrinogen to insoluble fibrin. New carboxylic groups were enzymatically generated in PET by the oxidoreductase laccase (EC 1.10.3.2). Treatment with nitrilase (EC 3.5.5.1) converted the nitrile groups in PAN into carboxylic acid groups (Pace and Brenner, 2001). Thrombin was finally immobilized on both fabrics by activating the newly generated carboxylic groups through 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide chemistry. The effect of the thrombin-functionalized fabrics on the recalcification time was assessed in vitro and in vivo confirming their ability to stop bleeding (Akkaya and Pazarlioglu, 2012). Collagen-based nanofiber meshes have been applied in tissue engineering using their capability to closely mimic the structure of the extracellular matrix (Rath et al., 2016; Law et al., 2017). In spinal cord injury treatment, microbial transglutaminase was utilized for grafting the neurotrophic factor neurotrophin-3 and the enzyme

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chondroitinase ABC, both protected with heparin, on electrospun (e-spun) collagen nanofibers. Transglutaminases (EC 2.3.2.12) catalyze the cross-linking of collagen and biomolecules with proteinaceous structure by formation of an isopeptide bond between the g-carboxamide group of glutamine and the ε-amino group of lysine (Keillor et al., 2014). The bioactivity assays revealed that the e-spun collagen nanofibers with incorporated neurotrophin-3 and chondroitinase ABC produced significant neurite outgrowth, because of the sustained release of neurotrophin-3 and prolonged enzymatic activity of chondroitinase ABC (Liu et al., 2012).

7.2.2

Sono-enzymatic fiber modification for incorporation of bioactives

Sonochemistry has been recognized as a green chemistry approach for synthesis and modification of materials. This method has found a broad spectrum of applications in engineering of nanomaterials, in water and wastewater treatments (Chen et al., 2012), and for enhancement of enzymatic reactions with nonnatural textile substrates (Bdalo et al., 2002; Huang et al., 2017). When high-power ultrasound propagates in a liquid, cavitation bubbles are generated because of pressure changes. The effect of cavitation as a consequence of the ultrasound action is several hundred times greater in heterogeneous than in homogeneous systems. The reason for this phenomenon is the forceful stirring of the otherwise relatively immobile liquid layer on the solide liquid interface, which in turn accelerates the accessibility of the enzyme to the textile surface (Eggleston and Vercellotti, 2007). The effect of ultrasound results in greater efficiency of the enzyme toward the nonnatural textile substrate, generating more functional groups on the fiber surface in a shorter reaction time. Following this rationale, our group sonochemically immobilized antimicrobial zinc oxide nanoparticles (ZnO NPs) on cotton fabrics by the involvement of a cellulase during the ultrasonication step. The boosted cellulase-mediated surface hydrolysis of the cotton fabric during sonication created reducing sugar ends, increasing the adhesion of the ZnO NPs and the antibacterial durability of the fabric. Around 33% of the ZnO NPs remained firmly embedded on the fabric after multiple high-temperature washing cycles. The textiles revealed high antibacterial activity against both Gram-positive and Gram-negative bacteria. The negligible antibacterial activity of the textiles observed when denaturated cellulase was introduced during sonication confirmed the importance of the enzymatic treatment for the antibacterial durability of the fabric (Petkova et al., 2016). This one-step process improved the previously published two-step procedure involving cellulase preactivation of the fibers followed by sonochemical deposition of ZnO NPs (Perelshtein et al., 2012). In a more recent work, cotton fabrics were upgraded with antibacterial ZnO NPs through the simultaneous application of ultrasound and the oxidative enzyme laccase. The rationale behind this sono-enzymatic approach was the in situ synthesis on enzymatic oxidation of gallic acid (GA) of a bioadhesive, in which the ZnO NPs were embedded. In absence of active laccase, the GA adhesive was not formed and the GA/ZnO NPs complex was progressively removed during washing. The sono-enzymatically functionalized fabric showed superior durability,

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retaining around 70% of its initial antibacterial effect after 60 washing cycles at high-temperature (75 C) hospital laundry regime (Salat et al., 2018).

7.3

Enzymes embedded on biomedical textiles

The application of enzymes has been widely recognized as a promising strategy for detection and (Rocchitta et al., 2016; Amine et al., 2016; Jha et al., 2008) treatment (Zhang et al., 2016; Liu et al., 2015; Kumar and Abdulhameed, 2017) of pathological conditions. Because of their high specificity, enzymes are capable of recognizing targeted substrates, which on their enzymatic conversion turn into products with either therapeutic benefit or bearing valuable bioanalytical information. However, enzymes are often characterized with short lifetime when applied in a free form and should be stabilized by immobilization (Malhotra and Chaubey, 2003). Immobilization of enzymes has shown several advantages over the use of free enzymes in solution, such as improved stability, specificity and selectivity, and reusability of the immobilized biocatalyst. Textile materials can be used as carriers for immobilization of enzymes by chemical or noncovalent interactions (Fig. 7.2). Generally, covalently immobilized enzymes offer higher reusability over the noncovalently incorporated ones. However, the chemical linkers used in the immobilization process are often toxic and can deteriorate the in vivo performance of the material. Avoiding harsh chemicals for enzyme immobilization on textiles will minimize potential immunological reactions. Thus, environmentally friendly techniques that apply mild conditions are desirable for enzyme immobilization onto biomedical textiles (Sakr and Borchard, 2013). TPFG; Linker; Negatively charged TPFG; Positively charged enzyme molecule; Negatively charged counterionic molecule; Textile

Electrospraying

(a)

Layer-by-layer

(b)

Figure 7.2 Strategies for immobilization of enzymes on biomedical textiles. (a) Noncovalent immobilization based on electrostatic interactions between negatively charged textile surface with positively charged enzyme molecules, and (b) Covalent immobilization of enzymes on textiles using a chemical linker.

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7.3.1

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Enzymes-embedded textiles for therapeutic application

Different examples illustrate how the immobilization of enzymes for therapeutic application resulted in high-performance devices that can assist and improve the disease treatment. Alkaline phosphatases (APs) (EC 3.1.3.1) are homodimeric metalloenzymes that hydrolyze the phosphoester bond in inorganic phosphates. They can be applied in the treatment of different pathological conditions such as hypophosphatasia (Millan, 2006). With this goal, Somerman et al. prepared nanofibrous fibrin scaffolds with covalently immobilized using carbodiimide chemistry alkaline phosphatase. The nanofibrous scaffolds incorporating AP served as a platform for treatment of hypophosphatasia, supporting in vitro differentiation and proliferation of osteoblast-like cell (Osathanon et al., 2009). In acute respiratory distress syndrome, the poor exchange of carbon dioxide can lead to increased levels in the bloodstream, related with high mortality rates (Boone et al., 2013). Immobilization of carbonic anhydrase (CA) (EC 4.2.1.1.) on the artificial lung membrane part of an extracorporeal carbon dioxide removal device is a promising strategy for facilitating carbon dioxide removal. HFMs made of various polymers can be used as a substrate for CA immobilization. CAs are zinc-dependent enzymes, which catalyze the reversible conversion of carbon dioxide to bicarbonate and protons (Supuran, 2008; Yadav et al., 2014). Fedespiel et al. immobilized CA on polymethylpentene hollow fiber membrane (HFM). The HFMs were preactivated through water plasma followed by cyanogen bromide treatment allowing for CA immobilization. The rate of carbon dioxide exchange from buffer increased by 75% compared with a control without immobilized enzyme. Furthermore, the authors tested the membrane for hemocompatibility and carbon dioxide removal in blood. The platelet deposition was decreased by 95% and the carbon dioxide removal rate was increased by 36% compared with unmodified HFM (Kaar et al., 2007; Arazawa et al., 2012). The same research group reported an improved enzymatically assisted method for CO2 removal by extracorporeal carbon dioxide removal device in patients with acute respiratory failure. In this case, CA was chemically immobilized on polymethylpentene HFM by using glutaraldehyde activated chitosan spacers (Arazawa et al., 2015). In a similar way, the filtration ability of HFM combined with the catalytic property of cholesterol oxidase (ChOx) (EC 1.1.3.6.), an enzyme that catalyzes the oxidative degradation of cholesterol and other sterols (Vrielink and Ghisla, 2009), resulted in hemodialysis membranes that allow removal of cholesterol for treatment of chronic kidney disease. ChOx was covalently immobilized onto PAN HFM using glutaraldehyde. Despite the amount of the immobilized enzyme increased with increasing the concentration of glutaraldehyde, the maximum activity of ChOx was determined at 10% glutaraldehyde cross-linker, indicating the limitations of this immobilization approach. After reusing 30 times the HFM, 58% of the initial ChOx activity was retained (Lin and Yang, 2003a,b). Similar to ChOx, urease (EC 3.5.1.5.), a nickel-dependent enzyme, which catalyzes the hydrolysis of urea to carbonic acid and ammonia (Sujoy and Aparna, 2013), has shown therapeutic potential in treatment of kidney failure (Yingjie and Cabral, 2002) by urea removal. Trochimczuk et al. studied the immobilization of urease on polysulfone membrane for removal of urea in artificial kidney systems. The enzyme

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was immobilized on the aminated polysulfone membrane by glutaraldehyde. The thermal and the storage stability of the enzyme were improved in addition to extending its pH-optimum range (Pozniak et al., 1995). For the same purpose, Lin et al. immobilized urease on PAN hollow fibers using glutaraldehyde. In this case maximum activity of urease was achieved when the PAN fibers were pretreated with 5% glutaraldehyde. The urea removal rate was improved by threefold compared with regular dialyzer (Yang and Lin, 2001). The same authors investigated the storage and operation properties of the covalently immobilized urea observing that the covalently immobilized enzyme retained 90% of its activity when stored for 42 days at pH 7. Similar residual activity (80%) was observed after 8 and 15 cycles of reuse (Lin and Yang, 2003c). In the treatment of infections, the combination of enzymes and biomedical textiles has shown high potential. Lysozyme (EC 3.2.1.17.), a well-known antibacterial enzyme present in many physiological liquids, i.e., sweat, saliva and tears, hydrolyzes the b-(1 / 4) linkages between N-acetylmuramic acid and N-acetylglucosaminealternating monomeric units of peptidoglycans. Peptidoglycans are important structural elements of the essential bacterial cell wall; therefore, the inclusion of lysozyme in medical textiles would contribute for prevention and treatment of infections. Wang et al. developed a wool fabric with antibacterial properties by immobilization of lysozyme using glutaraldehyde as a cross-linking agent. Optimum performance against S. aureus was achieved when the fabric was pretreated with 0.2% glutaraldehyde, followed by immobilization of the enzyme. However, the antimicrobial properties of the fabric showed limited durability at washing, retaining 43% of the initial enzyme activity after only five washing cycles (Wang et al., 2009). Lysozyme has also been immobilized on cellulose acetate e-spun nanofibers through noncovalent strategies such as electrospraying and LbL deposition. Using the e-spun cellulose acetate nanofibers as a negative substrate, a mixture of positively charged lysozyme and rectorite was deposited by electrospraying. A significantly enhanced antibacterial performance of the nanofibers against both Gram-positive and Gram-negative bacteria was observed (Li et al., 2014). LbL is a simple, flexible, and robust technique based on multilayer alternating deposition of oppositely charged polyelectrolytes, showing promising results for enzyme immobilization (Fig. 7.2) (Sakr and Borchard, 2013). LbL was applied to build lysozyme multilayer coatings on nanofibrous mats. The positively charged N-[(2-hydroxy-3-trimethylammonium) propyl] chitosan chloride (HTCC)/lysozyme composite and the negatively charged alginate were alternately deposited on the surface of e-spun cellulose acetate mats. Increasing the number of bilayers (from 5e5.5 to 10e10.5) and keeping the lysozyme/HTCC composite in the outermost layer resulted in increased antibacterial activity of the fibrous material against both Grampositive and Gram-negative bacteria (Huang et al., 2013). In a more recent example of LbL coating, negatively charged gold nanoparticles (AuNPs) and positively charged lysozyme were assembled on negatively charged cellulose mats. In this case, the outermost layer dramatically influenced the antimicrobial activity of the material against Gram-positive bacteria, observing a superior antibacterial activity in mats having lysozyme in the outermost layer, compared these with AuNPs. The authors concluded

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that the generated materials are appropriate for wound healing or tissue engineering applications (Zhou et al., 2014). The detoxification ability of certain enzymes can also be incorporated in medical textiles to prevent cells from oxidative damage. Catalase (EC 1.11.1.6), an enzyme catalyzing the dismutation of hydrogen peroxide (H2O2) to water and oxygen, was immobilized on cellulose acetate e-spun nanofibrous mats in an LbL fashion. The multilayers comprised negatively charged catalase and chitosan polycation. Maximum retained enzymatic activity (w42%) was achieved when 20 bilayers were deposited, which fact was attributed to the high porosity and surface area of the nanofibers. The authors observed significant protective effect of the membranes against H2O2induced cytotoxicity on human umbilical vascular endothelial cells (Huang et al., 2014). If there is a medical procedure where textiles have played an essential role since ancient times, this is wound treatment. However, the bioinert nature of the commonly used for wound dressing polymers requires their functionalization with bioactive molecules, which will eventually provide a more efficient wound treatment. Enzymes that were previously found to have positive effect on wound healing could be immobilized on dressings. Trypsine (EC 3.4.21.4), a serine protease found in the gastrointestinal tract of many vertebrates, has been used for debridement of either acute or chronic wounds (White et al., 2013; Shah and Mital, 2018). For the purposes of enzymatically assisted wound debridement, trypsine was immobilized on e-spun chitosan nanofibers through a one-step carbodiimide method, showing high proteolytic activity (Srbova et al., 2016).

7.3.2

Enzyme-embedded textiles for clinical diagnostics

Utilization of enzymes for measuring the concentration of different metabolites is a strategy widely applied in clinical diagnostics. HRP (EC 1.11.1.7), an oxidoreductase able to oxidize a large number of organic and inorganic substrates, has been exploited for measuring H2O2 concentrations, serving as a biomarker in clinical diagnostics of different diseases (Veitch, 2004). Baysal et al. immobilized HRP on polyester/nylon microfiber to fabricate a nonwoven textile-based biosensing platform for colorimetric detection of H2O2. Photolithography technique was used to fabricate the patterns, reservoirs, and channels followed by enzyme entrapment in gelatin. The linear working range of H2O2 was found to be 0.1e0.6 mM, and the system did not show deviation in a pH range of 3e7. The authors envisaged that this type of biosensing platform could be combined with various H2O2-producing enzymes, such as glucose oxidase (GOx), allowing fast detection of glucose (Baysal et al., 2015). Other enzymes, such as catalase, can also be used for measuring of H2O2 levels. Li et al. immobilized catalase on PAN and poly-(6-O-vinyl sebacoyl D-glucose) nanofibrous membranes using epichlorohydrin as coupling agent, improving the storage and temperature stability of the enzyme and broadening its pH range of activity. The authors envisaged various applications of the prepared nanofibrous membranes, including its utilization as biosensing platform (Li et al., 2012).

Enzyme

Fabric/fiber support

Immobilization method

Application

References

Alkaline phosphatase

Fibrin scaffold

Cross-linking (1-ethyl-(3dimethylaminopropyl) hydrochloride)

Osteoblast differentiation

Millan, 2006

Carbonic anhydrase

Poly(methylpentene)

Cyanogen bromide

Respiratory distress syndrome treatment

Kaar et al., 2007; Arazawa et al., 2012

Catalase

Cellulose acetate Polyacrylonitrile/poly(6-O-vinyl sebacoyl D-glucose)

Layer-by-layer Cross-linking (epichlorohydrin)

Protection from oxidative stress; Biosensing of hydrogen peroxide

Huang et al., 2014; Li et al., 2012

Cholesterol oxidase

Polyacrylonitrile Polyaniline/ polystyrene

Cross-linking (glutaraldehyde) Layer-by-layer

Chronic kidney disease; Detection of diseases, related with elevated levels of cholesterol

Lin and Yang, 2003a,b; Shin and Kameoka, 2012

Galactosidase

Poly(ε-caprolactone)/ a,u-azido-poly (ε-caprolactone)

Alkynyl-biotin

Vascular bypass surgery

Wang et al., 2015

Glucose oxidase

Nylon 6,6

Covalent bonds through aldehyde groups of PBIBA coating

Glucose biosensing/monitoring of diabetes

Uzun et al., 2014

b-Glucuronidase

Poly(vinyl alcohol)

Alkynyl-biotin/avidin

Enzyme prodrug therapy for cardiovascular grafts

Chandrawati et al., 2017

Horseradish peroxidase

Polyester/nylon

Entrapment in gelatin

Biosensing of hydrogen peroxide

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Table 7.1 Biomedical textiles with immobilized enzymes for therapeutic and bioanalytical applications.

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Table 7.1 Continued Enzyme

Fabric/fiber support

Immobilization method

Application

References

Lysozyme

Wool Cellulose acetate

Cross-linking (glutaraldehyde) Electrospraying Layer-bylayer

Treatment/prevention of bacterial infections

Wang et al., 2009; Li et al., 2014; Huang et al., 2013; Zhou et al., 2014

Trypsine

Chitosan

Cross-linking (carbodiimide/ N-hydroxysulfosuccinimide)

Wound debridement/wound care

Srbova et al., 2016

Urease

Polysulfone Polyacrylonitrile

Cross-linking (glutaraldehyde)

Chronic kidney disease

Pozniak et al., 1995; Yang and Lin, 2001; Lin and Yang, 2003c

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Elevated levels of cholesterol are indicative of different pathological conditions, such as neurological disorders, cardiovascular disease, and certain types of cancer (Watson and De Meester, 2016). To measure cholesterol levels in plasma, ChOx has been applied in a textile-based amperometric biosensor. Shin et al. combined electrospinning with LbL deposition. A polyaniline and polystyrene-blended e-spun mat served as a platform for electrostatic LbL deposition of the negatively charged ChOx and the polycationic poly(diallyldimethylammonium chloride) (PDDA). Rinsing in titanium butoxide solution increased the adhesion between the e-spun mat and PDDA. The e-spun/LbL-constructed biosensor showed high response accuracy to cholesterol when five bilayers were deposited (Shin and Kameoka, 2012). Urea levels are biomarkers for different diseases such as kidney disease (Weiner et al., 2014) and hyperammonemia (Braissant, 2010). Simon et al. prepared nanofibers for urea biosensing by electrospinning of urease-containing polyvinylpyrrolidone solutions. The prepared nanofibrous membranes showed faster response time, higher sensitivity to low urea concentrations, and are promising platforms for versatile biosensor design (Sawicka et al., 2005). Elevated concentrations of metabolite blood levels have been related to various pathological conditions. GOx (EC 1.1.3.4) is an oxidoreductase that catalyzes the oxidation of glucose to gluconic acid and hydrogen peroxide. The catalytic function of this enzyme has been used for the measurement of glucose concentration in blood (Bankar et al., 2009). Uzun et al. immobilized GOx on e-spun nanofibers of either nylon 6,6 or nylon 6,6/multiwalled carbon nanotubes coated with the conducting polymer (poly-4-(4,7-di(thiophen-2-yl)-1H-benzo[d]imidazole-2-yl)benzaldehyde) (PBIBA) to achieve highly electroactive surface area for GOx immobilization. It was demonstrated that the combination of the nanofibers and the electropolymerized PBIBA served as excellent immobilization matrix with a long period stability, which resulted from the robust covalent bonds between the GOx and the aldehyde groups of the conducting polymer used as a coating on the nanofibers’ surface. The resulting material revealed low detection limit and high affinity to glucose. The authors envisaged the application of the proposed method to develop different e-spun nanofiberebased biosensors for measurement of other metabolites (Uzun et al., 2014). GOx was incorporated on poly(vinyl alcohol) (PVA)/polyethyleneimine composite nanofibers by dissolving the enzyme in the polymer blend solution, before electrospinning. The conductive properties of the NFs were significantly improved by decoration with previously prepared gold NPs, evidenced with cyclic voltammetry. The response was linear in the 10e200 mM range, coupled with very low limit of detection (0.9 mM), and the biosensor exhibited good operational and storage stabilities (Sapountzi et al., 2017). Fang et al. built minimally invasive glucose biosensor for measuring glucose blood levels in diabetes mellitus patients. The previously electropolymerized polyaniline nanofibers deposited in the form of thin film on the working electrode were used as a substrate for immobilization of GOx through cross-linking with glutaraldehyde. After that, to increase the biocompatibility of the implantable biosensor, layers of polyurethane and epoxy-polyurethane (PU/PU-E) were deposited onto the polyaniline nanofibers. The PU membrane provided balance between oxygen and glucose

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transport to the sensing part, while the PU-E enhanced the durability of PU membrane and improved the stability of the protective layer. In vivo experiments showed high responsiveness of the biosensor to variations of the blood glucose and continuous and steadily performance within the 26 days timeframe (Fang et al., 2017). The demand for simultaneous determination of several metabolites has lead to the development of textile-based devices incorporating multiple enzymatic activities. For example, a polyester thread-based microfluidic system with immobilized urease, GOx, and HRP was created for the simultaneous detection of urea nitrogen and glucose levels in blood. The biosensing device showed good electroosmotic and flow mobility compared with conventional glass microfluidic channels (Yang and Lin, 2015).

7.3.3

Enzyme-embedded textiles for enzyme prodrug therapy

Finally, enzyme-embedded textiles have demonstrated potential for enzyme prodrug therapies based on bioconversion of the inactive form of a drug into the active one by a specific enzyme present in a body tissue (Walther et al., 2017). Textiles with immobilized enzymes can be applied locally and convert on-site the administered prodrug into its active form to achieve the desired therapeutic effect. Moreover, this strategy allowed for using enzymes from nonhuman sources, i.e., b-galactosidase from Escherichia coli known as a stronger catalyst with higher turnover rate, compared with the mammalian homologue (Fejerskov et al., 2017). Wang et al. fabricated e-spun fibers by blending poly(ε-caprolactone) (PCL) and a,u-azido-poly (ε-caprolactone) (PCL-N3) for vascular bypass surgery. The PCL surface was biotinylated through click reaction between azide groups and alkynyl-biotin. The high affinity between avitin and biotin was used to immobilize E. coli b-galactosidase. b-Galactosidase (EC 3.1.2.23) is a hydrolytic enzyme, which catalyzes the reaction of decomposition of lactose to galactose and glucose (Matthews, 2005). In this case, the catalytic activity of b-galactosidase was used to catalyze the hydrolysis of b-gal-NONOate prodrug, which on bioconversion gives two molecules of nitric oxide (NO). The prepared vascular grafts were evaluated in vitro for their ability to catalyze the decomposition of NO prodrug and in vivo for physiological function performance. The immobilized enzyme retained its activity for up to 1 month after implantation, during which period the sustained release of NO inhibited platelet adhesion and thrombus formation and improved tissue regeneration and remodeling. The authors considered this strategy superior to the traditional NO drugeloaded delivery system (Wang et al., 2015). In another example of prodrug therapy for cardiovascular grafts, b-glucuronidase (EC 3.2.1.31), an enzyme that catalyzes the hydrolysis of b-D-glucuronic acid residues from the nonreducing end of mucopolysaccharides, was encapsulated in liposomes and further immobilized on PVA e-spun nanofibers. The liposomes provided the desired stabilization of the enzyme during manufacturing and storage and served as a protective shield for proteolytic degradation and loss of activity in cell culture media. The nanofibers were bioactive during 7 weeks. The therapeutic utility of the prepared nanofibers was validated by using externally administrated prodrug SN-38-glucuronide, which on enzymatic action was converted into the active antiproliferative form SN-38 (Chandrawati et al., 2017).

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Enzyme-responsive biomedical textiles

Stimuli-responsive materials are emerging as promising candidates for application in various biomedical areas, such as diagnostics, tissue engineering, drug delivery, and cell culture (Xu et al., 2016; Hoffman, 2013). A wide range of chemical, physicochemical, or biological stimuli, such as temperature, pH, light, electric and magnetic fields, ultrasound, mechanical stress, ions, and enzymatic activity, can be engaged from the environment or the human organism to trigger material responsiveness and induce positive biochemical or physiological reaction in the targeted tissue (Cao and Wang, 2016; Chan et al., 2013). Among these stimuli, enzymes have attracted great interest in the biomedical field because of a relatively large deviation from their normal activity in various human pathologies. Enzymes can serve as a drug delivery trigger cleaving enzyme-sensitive linkers or degrading bulk materials on the site of administration. The enzymatic action alters the chemical, physicochemical, or biological properties of the material causing subsequent release of the bioactive therapeutic or analytical compound. Therefore, enzyme activity on the application site is an important parameter to be considered in the design of drug delivery materials to achieve controlled response behavior. This section overviews textile material, which responsiveness can be triggered in situ by enzymes produced in the targeted tissue on pathological conditions or by externally supplied enzymes. Enzymatically induced responsiveness of textile materials can be achieved in two ways: (1) by tailoring the chemical structure of the textile polymer introducing enzymatically degradable chemical groups (Fig. 7.3(a)) and (2) by using enzymatically

(a) Fabrication step

(b)

Application step Enzymatically degraded textile; Enzymatically cleavable linker; Bioactive molecule; Enzyme; TPFG. Fabrication step

Application step

Figure 7.3 Strategies for the development of enzymatically responsive biomedical textiles: (a) Tailoring the textile chemical structure for incorporation of bioactive molecules (fabrication step) which are released on enzymatic textile degradation on the site of action (application step). (b) The bioactive molecule of interest is immobilized on the textile support through enzymatically cleavable linker (fabrication step) which is scissed on enzyme action, triggering the payload release (application step).

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cleavable linkers, which function is to serve as anchors of bioactive molecules on the textile support (Fig. 7.3(b)). In the first case, the molecule of interest is incorporated in the textile structure and released on enzymatic degradation of the fibrous polymer, whereas in the second case the active molecule is released through degradation of the enzymatically cleavable linker, without altering the integrity of the textile support. In medicine, biodegradability, as a type of responsiveness, is a highly desirable biofeature that can be used for precise administration of bioactives. The biodegradability profile of the polymers is a crucial factor when choosing the matrix in which the active compound will be incorporated (Dash and Konkimalla, 2012; Laycock et al., 2017). For instance, fast biodegradation of polymers for long-term implantable materials is not desirable because the continuous change of the materials’ mechanical properties because of the bioerosion can deteriorate its characteristics and its in vivo performance. On the other hand, in many biomedical applications and especially in the area of drug delivery, controllable biodegradation is often preferred so that the drug of interest can be released in a sustained manner on degradation of the material (Nair and Laurencin, 2007; Tian et al., 2012).

7.4.1

Textile-responsive strategies based on enzymatic degradation

Enzymatically degradable poly (L-lactic acid) (PLLA) e-spun nanofibers were investigated for their potential application as drug delivery systems. The observed sustained release of the model drug rifampin from the e-spun platforms on addition of proteinase K (EC 3.4.21.64) was attributed to the enzymatically mediated PLLA degradation rather than drug diffusion (Zeng et al., 2003). Biodegradable polyurethane materials (Cherng et al., 2013; Cooper and Guan, 2016) have been modified with chain extenders susceptible to enzymatic attack. This strategy has been used to produce e-spun polyurethane microfibers with chymotrypsin (EC 3.4.21.1) cleavable segments, useful for gastrointestinal tissue engineering. In tissue engineering, the biodegradability in many cases is a highly desired feature of the materials, and in this way the material is gradually dissolved and further resorbed and metabolized/excreted of the human organism without the need for additional surgery for its removal (Ramakrishna et al., 2017; Iqbal et al., 2018; Joseph et al., 2015). Although no significant weight loss of the e-spun polyurethane microfibers was detected after exposure to chymotrypsin for up to 28 days, the morphology of the treated fibers was altered, which the authors assigned to their susceptibility to enzymatic degradation (Rockwood et al., 2007). Later, the same authors inserted a glycineleucine (Gly-Leu)ebased chain extender into polyurethane macromolecules to create matrix metalloproteinases (MMPs) (EC 3.4.24.) degradable e-spun nanofibers for soft tissue engineering. However, in this study, solely the viability of fibroblast cell culture was investigated without evaluating the interaction of the nanofibers with MMPs (Parrag and Woodhouse, 2010). Wound healing fibrous materials can be designed by insertion of enzyme-cleavable peptide sequence for in situ degradation by externally introduced collagenase

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(EC 3.4.23.3). Such materials were used in a synthetic capillary delivery system for burns and chronic wound healing where the capillaries dissolve after the therapeutic period on activity of externally introduced collagenase. To design the collagenasedegradable textile device, Fu et al. introduced a collagenase-sensitive peptide as a chain extender into polyurethane urea elastomers. Afterward, the copolymer was espun into a fibrous conduit to obtain HFM. These HFM were disintegrated within 3 days on exposure to collagenase (Fu et al., 2014).

7.4.2

Textile-responsive strategies based on enzymatically cleavable linkers

The use of enzymatically degradable polymers is not desirable in textile-based platforms for biosensing applications because the degradation of the platform might deteriorate the performance of the medical device. In such cases, bioactive molecules are immobilized on the textile polymer via enzymatically cleavable linkers, which on enzymatic attack release these bioactives to the environment to obtain the desired signal or physiological outcome. Following this rationale, textiles for the purpose of gene therapy have been produced. Elevated levels of calcium-dependent zinccontaining MMPs in chronic ulcers lead to excessive degradation of the extracellular matrix constituents. Control over MMP activity in the wound bed could have beneficial outcomes for the wound healing process. In this sense, reduced MMPs gene expression and therefore activity have been achieved using e-spun nanofibrous mats with immobilized gene expression controlling molecules such as DNA plasmids and small interfering RNA. An MMP-cleavable heptapeptide was immobilized on the amino groups of e-spun nanofiber mats from PCL and amine-terminated poly(ethylene glycol) block copolymer, through N-(3-dimethylaminopropyl)-Nethylcarbodiimide hydrochloride and N-hydroxysuccinimide chemistry to form a carbamate linkage. Afterward, linear polyethylenimine (LPEI), previously activated with N-succinimidyl-3-(2-pyridyldithio)propionate, was conjugated to the nanofibers through reaction with the thiol group of cysteinyl residue, located on the free end of the MMPs-cleavable heptapeptide. Finally, negatively charged plasmid DNA, siRNA, or plasma human epidermal growth factor (phEGF) was incorporated in the nanofibers through electrostatic interaction with the positively charged LPEI. The activity of wound MMPs induced the release of LPEI from the e-spun nanofiber mats, necessary for the cell transfection of the gene expression controlling molecules, thus promoting wound healing in an animal model (Kim and Yoo, 2010, 2013; Sung and Sang, 2013). Textiles in the form of e-spun mats have been used also for delivery of small molecules. Nitric oxide (NO) influences several important factors for wound healing functions, such as angiogenesis, matrix deposition, inflammation, cell proliferation, and remodeling (Luo and Chen, 2005). Zhao et al. combined e-spun PCL mat with NO prodrug galactose-N-diazeniumdiolateegrafted chitosan (CS-NO) to prepare wound dressing, which released NO in the wound bed on galactosidase action. Initially, the e-spun mat was hydrolyzed in aqueous alkaline solution to increase the

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surface bonding and after that the e-spun mat was coated with CS-NO by drop casting. In vitro experiments demonstrated a sustained release over 72 h of NO in presence of the enzyme, while in vivo studies with mice models showed significantly accelerated wound closure (Zhou et al., 2017d). Finally, immobilization of fluorescently labeled enzymatically cleavable peptides on textile carriers is an interesting approach to monitor enzymes in biological fluids for diagnostic purposes. This method, based on fluorescence emission on enzymatically induced cleavage of the peptide, can be employed for detection of enzymes at levels as low as the picomolar range (Drake et al., 2013). Detection of MMP-9 (gelatinase-2) (EC 3.4.24.35) could improve the early diagnosis of many diseases (Yabluchanskiy et al., 2013; Farina and Mackay, 2014; Gr€unwald et al., 2016; Rayment et al., 2008). For this purpose, a textile microdevice was fabricated for highly sensitive MMP-9 detection comprising fluorescein isothiocyanateelabeled MMP9ecleavable peptides onto poly(styrene)/poly(styrene-alt-maleic anhydride) e-spun nanofibers. Before peptide immobilization, the nanofiber matrix was incorporated into hydrogel micropatterns for easy size control and handling of the nanofiber material. Thereafter, the resultant hydrogel-framed nanofiber matrix was inserted into a microfluidic device equipped with reaction chamber and detection zones. In the reaction chamber, specific interaction between MMP-9 and the immobilized peptides occurred, leading to generation of a fluorescent signal visualized in the detection zone. When higher concentrations of MMP-9 or larger peptideimmobilizing nanofiber areas were used, the stronger was the detected fluorescent signal. The large surface area of the nanofibers and small dimensions of the microsystem allowed for a response time of 30 min and a detection limit down to 10 p.m. The hydrogel-embedded nanofiber matrix in this device is disposable and can be replaced with either the same or different immobilized biomolecules, while the microfluidic system is reusable (Han and Koh, 2016). Also, based on the fluorogenic peptide cleavage approach, dressings were modified for the detection of human neutrophil elastase (HNE) (EC 3.4.21.37), a serine protease was found in elevated levels in chronic wounds. HNE degrades elastin in human skin and thus could be considered as a reliable marker of inflammation in early stages of wound chronification. A short cleavable peptide was coupled to a fluorescence-quenching system based on F€ orster resonance energy transfer (FRET) for a more sensitive detection. The FRET system was based on the fluorophore donors N-(aminoethyl)-5naphthaleneamine-1-sulfonic acid (EDANS) and the quencher acceptor dabcyl (4-([40 -dimethylamino)phenyl]azo)benzoyl], covalently linked to the N- and C-terminals of the peptide substrate, respectively. Glutaraldehyde-activated FRET peptide was immobilized on polyamide dressing pretreated in alkaline conditions. Despite HNE inducing an enhanced fluorescent signal with the EDANS/Dabcyl FRET peptide, its chemical immobilization onto the polyamide dressing greatly decreased its detection, mainly because of the more difficult access of the enzyme to the cleavage sequence of the immobilized peptide. The authors suggested that further improvement of the immobilization procedure would improve the HNE detection capabilities of the textile-based device (Ferreira et al., 2017).

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Conclusions and future trends

Nowadays, the term “biomedical textiles” has a broad definition. Fibers can be found as constituents of a wide range of medical tools, from surgical sutures to HFMs in artificial lungs, or microfluidic platforms in biosensors. The research reviewed here shows how, through enzyme biotechnology, known “biomedical textiles” can be upgraded with new biofunctionalities or new medical tools not achievable through other strategies. However, this is an emerging field and despite some reported success the novel generated materials are still far from the end users. Some biotechnological materials reviewed here showed promising in vitro efficacy; however, proper clinical studies to demonstrate the material efficacy in the application environment are still needed. Other examples are still proof of concepts and that despite the authors provide an attractive novel biotechnological textile material they have not established a defined application. Ultimately, the material manufacturing will be a key step to close the gap between the developers and the end users. In this sense, the combination of biotechnological approaches with different scalable additive technologies such as electrospinning, electrospraying, ultrasonication, or LbL deposition emerge as a promising approach to translate the lab-produced materials into prototypes for further studies and eventually reach the end users. As future trends, the medical advances in disease detection and treatment will drive the development of new biotechnological textiles. On the other hand, novel enzymes, because of discovery or genetic engineering, will represent new tools for textile modification or highly stable catalyst to confer biofunctionalities for medical applications.

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