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Hydrogels Based on Schiff Base Linkages for Biomedical Applications

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molecules Review Hydrogels Based on Schiff Base Linkages for Biomedical Applications 1, 1, 1,2, Junpeng Xu y, Yi Liu y and Shan-hui Hsu * 1 Institute of Polymer Science and Engineering, National Taiwan University, No. 1, Sec. 4 Roosevelt Road, Taipei 10617, Taiwan 2 Institute of Cellular and System Medicine, National Health Research Institutes, No. 35 Keyan Road, Miaoli 35053, Taiwan * Correspondence: [email protected]; Tel.: +886-2-3366-5313; Fax: +886-2-3366-5237 These authors contributed equally to this paper. y Received: 19 July 2019; Accepted: 13 August 2019; Published: 19 August 2019 Abstract: Schiff base, an important family of reaction in click chemistry, has received significant attention in the formation of self-healing hydrogels in recent years. Schiff base reversibly reacts even in mild conditions, which allows hydrogels with self-healing ability to recover their structures and functions after damages. Moreover, pH-sensitivity of the Schiff base offers the hydrogels response to biologically relevant stimuli. Different types of Schiff base can provide the hydrogels with tunable mechanical properties and chemical stabilities. In this review, we summarized the design and preparation of hydrogels based on various types of Schiff base linkages, as well as the biomedical applications of hydrogels in drug delivery, tissue regeneration, wound healing, tissue adhesives, bioprinting, and biosensors. Keywords: Schiff base; hydrogel; click chemistry; self-healing; dynamic covalent bond; tissue engineering 1. Introduction Hydrogels with a three-dimensional structure and high water content are an important category of soft materials [1,2]. Hydrogels provide a physiologically similar environment for cell growth and they are often used to mimic the extracellular matrix (ECM) [3]. Cells interact and remodel with the ECM or ECM-like structures to achieve various cell behaviors, such as proliferation [4], migration [5], and differentiation [6]. Therefore, hydrogels have been developed for several biomedical applications [7], including tissue engineering [8], wound dressing [9], and drug delivery [10]. Hydrogels are generally formed by connecting hydrophilic polymer chains with various kinds of linkages to form networks [7]. The crosslinking network is divided into two types, i.e., the covalent network and non-covalent network, based on the nature of the linkages [11]. Click chemistry is one of the most common reactions used to obtain a covalent hydrogel network [12]. Click chemistry, initially proposed by Sharpless et al. in 2001, is a strategy combining various units to create highly selective products with a reliable high yield and effective atom utilization [13]. Click chemistry can yield smart materials that respond to external stimuli, and are often used as a key tool to prepare covalently crosslinked hydrogels for biomedical applications [14]. Typical examples of click chemistry are the Huisgen cycloaddition reaction [15], thiol-ene reaction [16], Diels–Alder reaction [17], Michael addition reaction [18], and the Schiff reaction [19]. These click reactions have been widely used in materials science [20–22], life sciences [23], and polymer chemistry [24,25]. Efficient click reactions in polymer chemistry have led to the development of new synthetic strategies. Click reactions can effectively create condensed polymers, as well as modify polymer chains and sophisticated architectures, including smart hydrogel networks or scaffolds. The Schiff reaction is a Molecules 2019, 24, 3005; doi:10.3390/molecules24163005 www.mdpi.com/journal/molecules Molecules 2019, 24, x FOR PEER REVIEW 2 of 22 Molecules 2019, 24, 3005 2 of 21 sophisticated architectures, including smart hydrogel networks or scaffolds. The Schiff reaction is a family of reactions used to generate dynamic Schiff base linkages, and it is currently one of the best methodsfamily of to reactions prepare usedsmart to biocompatible generate dynamic hydrogels. Schiff base linkages, and it is currently one of the best methodsThe toSchiff prepare reaction smart is biocompatiblea chemical reaction hydrogels. involving a dynamic covalent imine bond formation via theThe crosslinking Schiff reaction of amine is a chemical groups reactionand aldehyde involving groups a dynamic [26]. Schiff covalent base linkages imine bond can formationbe generated via inthe situ crosslinking with cells, of tissues, amine groupsand bioactive and aldehyde molecules groups under [26]. physiological Schiff base linkages conditions can beto generatedcreate hydrogel in situ withnetworks. cells, tissues,The dynamic and bioactive crosslinking molecules networks under can physiological also give hydrogels conditions their to create self-healing hydrogel properties networks. The[27].dynamic Moreover, crosslinking the Schiff networksbase is pH-responsive can also give hydrogels according their to its self-healing chemical structure properties [28]. [27]. Schiff Moreover, base linkages,the Schiff baseincluding is pH-responsive imines, hydrazones, according toand its oximes chemical, are structure the products [28]. Schi offf basecondensation linkages, includingreactions betweenimines, hydrazones, aldehyde groups and oximes, and various are the nucleophilic products of condensationamine groups. reactions Compared between to imines, aldehyde oximes groups and hydrazonesand various have nucleophilic better chemical amine groups. stability Compared with pH tovalue imines, changes oximes because and hydrazones the mesomeric have bettereffect reduceschemical the stability electrophilicity with pH of value the original changes carbon–nitrogen because the mesomeric double bond effect [28]. reduces Hydrogels the electrophilicity with various Schiffof the base original linkages carbon–nitrogen have unique double properties bond to [28 m].eet Hydrogels the requirements with various of different Schiff base tissues. linkages The Schiff have reactionunique propertieshas excellent to meet prospects the requirements in the biomedical of different field tissues.due to Theits simplicity, Schiff reaction reversibility, has excellent pH- prospectssensitivity, in and the biocompatibility. biomedical field due to its simplicity, reversibility, pH-sensitivity, and biocompatibility. Hydrogels with Schiff Schiff base linkages are currently used in several biomedical fields fields (Figure (Figure 11),), including drugdrug deliverydelivery [ 29[29,30],,30], tissue tissue regeneration regeneration [31 [31,32],,32], wound wound healing healing [33 ,[33,34],34], tissue tissue adhesives adhesives [35], [35],bioprinting bioprinting [36], and[36], biosensors and biosensors [37]. This [37]. review This review highlighted highlighted the use the of diusefferent of different Schiff base Schiff linkages base linkagesas crosslinking as crosslinking strategies strategies to prepare to biologically prepare biol relevantogically hydrogels relevant that hydrogels can be usedthat incan physiological be used in physiologicalenvironments. environments. After a brief classification After a brief of theclassification Schiff base, weof the summarized Schiff base, the chemicalwe summarized mechanisms the chemicalof different mechanisms linkages. The of preparationdifferent linkages. and biomedical The preparation applications and of hydrogelsbiomedical based applications on the Schi offf hydrogelsreaction were based further on the epitomized. Schiff reaction were further epitomized. Figure 1. SummarySummary of of biomedical biomedical applications applications for for hydr hydrogelsogels based on various Schiff Schiff base linkages. 2. Design Design and and Preparation Preparation The Schiff Schiff base formation is obtained via the nucleophilicnucleophilic attack of amines on the electrophilic carbon atoms of aldehydes or keto ketones.nes. Hydrogels Hydrogels for biomedical applications have been extensively developed based on iminesimines andand theirtheir derivatives,derivatives, includingincluding hydrazoneshydrazones andand oximes.oximes. Imines, hydrazones, and oximes are formed by reaction between aldehydes/ketones aldehydes/ketones and primary amines, amines, hydrazides, and aminooxy, respectively. Hydrazones and and oximes exhibit better intrinsic stability compared to imines. Furthermore, Furthermore, acylhydrazones acylhydrazones allow allow higher higher hydrolytic hydrolytic stability compared to hydrazones and oximes [38]. [38]. In several recent st studies,udies, hydrazones and acylhydrazones with proper Molecules 2019,, 24,, 3005x FOR PEER REVIEW 33 of of 2122 stability were employed to form crosslinks in hydrogel networks. Moreover, benzoic Schiff base stabilitylinkages werehave been employed widely to studied, form crosslinks where the in stab hydrogelility of networks. carbon–nitrogen Moreover, double benzoic bonds Schi hasff beenbase linkagesimproved have through been aromatic widely studied, substitution where with the stabilitybenzene ofrings carbon–nitrogen connected to doublethe carbon bonds or hasnitrogen been improvedatoms [39]. through Commonly, aromatic benzoic substitution Schiff base with linkages, benzene including rings connectedbenzoic imines, to the benzoic carbon hydrazides, or nitrogen atomsand benzoic [39]. Commonly, oximes, are benzoic formed Schi viaff linkagesbase linkages, of benzoic including aldehydes benzoic with imines, amines, benzoic hydrazides, hydrazides, and andaminooxy’s, benzoic respectively. oximes, are formed via linkages of benzoic aldehydes with amines, hydrazides, and aminooxy’s,Usually, respectively. chemical modifications are necessary
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