Development of Self-Healing Double-Network Hydrogels

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Cite This: J. Agric. Food Chem. 2019, 67, 6508−6516

Development of Self-Healing Double-Network Hydrogels: Enhancement of the Strength of Wheat Gluten Hydrogels by In Situ Metal−Catechol Coordination Chengzhen Liu,† David Julian McClements,‡ Man Li,† Liu Xiong,† and Qingjie Sun*,† †

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College of Food Science and Engineering, Qingdao Agricultural University, 700 Changcheng Road, Chengyang District, Qingdao, Shandong 266109, People’s Republic of China ‡ Department of Food Science, University of Massachusetts Amherst, Amherst, Massachusetts 01060, United States S Supporting Information *

ABSTRACT: Wheat gluten, a byproduct of the wheat starch industry, is widely used as a dough strengthener and gelling agent. In this research, we developed novel double-network hydrogels by gelation of gluten using in situ metal−catechol coordination. The first network consisted of physically associated gluten molecules, while the second network consisted of Fe3+-cross-linked proanthocyanidins (PACs). Dynamic shear rheology experiments suggested that coordination of Fe3+ and PACs greatly enhanced the mechanical properties of the gluten hydrogels. The double-network hydrogels exhibited a 3-fold higher shear modulus than pure gluten hydrogels. The formation of bis- and tris-catechol−Fe3+ complexes between Fe3+ and PACs in the hydrogels was confirmed by ultraviolet−visible spectrometry and isothermal titration calorimetry (ITC). The ITC measurements of Fe3+ binding to PACs indicated a molar stoichiometry of 1:4 and a dissociation constant (KD) of 24.9 × 10−9. When subject to repeated shear deformation−compression cycles, the hydrogels exhibited strong and rapid recovery of their rheological properties. The strong, self-healing characteristics of the double-network gluten hydrogels produced in this study may be useful for certain applications in the food, agriculture, biomedicine, and tissue-engineering industries. KEYWORDS: gels, polyphenols, viscoelastic properties, self-healing, soft matter

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relaxation times in wheat gluten hydrogels.9 Recently, it has been reported that sorghum-derived proanthocyanidins (PACs) dramatically increased the strength of wheat gluten doughs without negatively impacting their extensibility, which may be advantageous for certain commercial applications.10 The mechanical properties of hydrogels can be modulated using double-network hydrogels rather than single-network hydrogels. Double-network hydrogels consist of two interpenetrating networks of gelling materials, which is typically achieved using two polymers, one stiff and brittle and the other soft and flexible.11 Recently, it has been reported that dualnetwork poly(acrylamide-co-acrylic acid) hydrogels with toughness, ultrahigh mechanical strength, and good selfrecovery could be created using Fe3+ ions as cross-linking agents.12 A similar approach was used to create self-healing poly(acrylic acid) dual-network hydrogels with enhanced durability and mechanical performance but using cerium ions as cross-linkers.13 PACs are a group of bioactive polyphenol compounds extracted from fruits, wine, tea, and coffee.14 PACs have been used as nutraceuticals in functional foods because of their potential to inhibit chronic diseases, which has been partly attributed to their strong antioxidant and anti-inflammatory activities.15 As catechol-rich polymeric materials, PACs can

INTRODUCTION Hydrogels assembled from natural biopolymers, such as proteins and polysaccharides, are typically nontoxic, biocompatible, and biodegradable, which are beneficial for many purposes in the food, agriculture, and biomedical fields.1 Wheat gluten is a byproduct of wheat starch production that is a relatively cheap plant-based functional protein, consisting of about 50% monomeric gliadins and 50% polymeric glutenins.2 Wheat gluten is generally recognized as safe (GRAS) by the U.S. Food and Drug Administration (FDA), but certain segments of the population should avoid its consumption because of gluten intolerance or celiac disease. As a functional ingredient, gluten has been used as a dough strengthener, a stabilizing agent, a nutrient supplement, and a gelling agent as well as for various other functional purposes.3 The potential applications of gluten in bioactive delivery, packaging materials, and tissue engineering have also been explored.4 Gluten gels are composed of a complex mixture of wheat storage proteins that are held together by both physical and covalent interactions, including van der Waals forces, hydrogen bonding, hydrophobic interactions, π−π stacking, electrostatic interactions, and disulfide bridges. The poor mechanical properties of conventional gluten hydrogels, however, significantly limit their range of applications. Extensive studies have therefore been conducted to better understand the molecular−structural−mechanical basis of the rheological properties of gluten hydrogels, which is being used to enhance their functional performance.5−8 For example, cysteine incorporation leads to more rigid structures and longer © 2019 American Chemical Society

Received: Revised: Accepted: Published: 6508

March 13, 2019 April 30, 2019 May 21, 2019 May 22, 2019 DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

Article

Journal of Agricultural and Food Chemistry

Figure 1. (A) Storage modulus (G′) (solid symbols) and loss modulus (G″) (hollow symbols) and (B) tan δ of single-network gluten gels (SNGGs) and double-network gluten gels (DNGGs) as a function of angular frequency. approximately 80% protein content was provided by Shanghai Jin Jing Chemical Co., Ltd. (Shanghai, China). All other reagents were of analytical grade. 2.2. Preparation of Wheat Gluten Hydrogels. Wheat gluten hydrogels were prepared using a method described previously, with some modification.23 In a typical experiment, 5 g of wheat gluten was dispersed in 15 mL of distilled water at 25 °C and then the system was adjusted to pH 7 using small aliquots of either acid or base solution (1 M NaOH or 1 M HCl). The suspension was subsequently incubated at a fixed temperature (20, 30, 40, or 50 °C) for 30 min and then kept in an ice−water bath for 12 h to form the gluten hydrogel. 2.3. Preparation of Fe3+−PAC Double-Network Gluten Hydrogels. Initially, 5 g of wheat gluten was dispersed in 10 mL of distilled water at room temperature. Then, FeCl3 and PACs (5 mL) were mixed at a ratio of 1:2, 1:3, 1:4, 1:5, and 1:6 (w/w). This mixture was then added to the whey gluten dispersion immediately after the solution was vigorously mixed using a vortex mixer. This procedure yielded the following final concentrations of FeCl3 (0.06− 0.20 mg mL−1) and PACs (0.10−1.80 mg mL−1) in the dispersions. The suspension was then adjusted to pH 2.0, 4.0, 6.0, 8.6, 9.6, or 12.0 with different pH buffer solutions (1 M NaOH or 1 M HCl). Afterward, it was incubated for 30 min at fixed temperatures (20, 30, 40, or 50 °C) and then kept in an ice−water bath for 12 h to produce double-network gluten hydrogels. 2.4. Dynamic Rheological Measurements. The dynamic shear rheology of the double-network gluten hydrogels was characterized with an oscillating rheometer (MCR102, Anton Paar, Austria) at 20 °C, using a parallel plate system, with a diameter of 50 mm and gap of 1 mm. 2.4.1. Frequency Sweeps. The storage (G′) and loss (G″) moduli were measured by carrying out frequency sweeps over an angular frequency range of 0.1−100 rad/s, with constant deformation and a strain amplitude of 1% (within the linear viscoelastic region). 2.4.2. Self-Healing Properties. Rheological assessment of the selfhealing ability of the double-network gluten hydrogels was carried out using the following procedure. Hydrogels were prepared by mixing FeCl3 (0.5 mM) and PACs (2 mM) at the Fe3+/PAC ratio of 1:4 (pH 2.0, 4.0, 6.0, and 8.6). These samples were then immediately transferred to cylindrical casts and measured. In a nonlinear time sweep experiment, G′ and G″ of the hydrogel were initially recorded at 1% strain for 100 s and then a sudden strain of 1000% was applied for 100 s to compress the gel.22 The samples were then decompressed and compressed again repeatedly using the same conditions. These experiments were carried out at a fixed angular frequency of 10 rad s−1. 2.5. Morphology Observation. Wheat gluten hydrogel and double-network gluten hydrogels were cut into small pieces (1 mm3)

interact with metal ions to form metal−catechol coordination complexes, which are suitable for incorporation into particles or films.16 For instance, porous and hollow tea polyphenol-rich spheres have been fabricated by Cu2+-mediated oxidative coupling, which have potential for utilization as delivery systems for drugs and other bioactive agents.17 The formation of complexes between catecholic ligands and Fe3+ is one of the most widely observed metal−ligand interactions in nature.18,19 Under neutral or alkaline conditions, two or three galloyl groups from polyphenols can react with each Fe3+ ion to form a stable octahedral complex. These interactions can be used to create edible functional materials. For instance, cross-linked films have been formed by reacting tannic acid with Fe3+ ions.20 Moreover, cross-linked hydrogels have been formed by reacting catechol-modified polyethylene glycol polymers with Fe3+ ions.21 The resulting hydrogels are shown to have high elastic moduli and good self-healing properties. Moreover, cross-linked hydrogels with desirable rheological characteristics have been formed by reacting catechol-modified chitosan with either Fe3+ or Cu2+ ions.22 Despite the fact that cross-linking catechol-modified biopolymers with multivalent mineral ions can improve gel properties, its widespread utilization is limited because it is a time-consuming process that involves synthetic chemical reactions. In the present work, we developed a simple and rapid method of fabricating double-network gluten hydrogels based on physical interactions between gluten, PACs, and FeCl3. Our aim was to improve the mechanical performance of the hydrogels using an approach that might be suitable for the development of foods and other soft materials. For this reason, we examined the impact of system composition and processing parameters on the formation of the double-network gluten hydrogels. Furthermore, the morphology, rheology, and selfhealing characteristics of the double-network hydrogels were investigated. The results of this study may lead to the creation of a new class of materials that can be used to form gels, films, or delivery systems suitable for application in a broad range of industries.

2. MATERIALS AND METHODS 2.1. Materials. PAC (>98% purity) was purchased from Xi’an Nansi Biotechnology Co., Ltd. (Xi’an, China). Wheat gluten with 6509

DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

Article

Journal of Agricultural and Food Chemistry

Figure 2. (A) Storage modulus (G′) and loss modulus (G″) of single-network gluten gels (SNGGs) and double-network gluten gels (DNGGs) versus different incubation temperatures at a constant frequency of 10 rad/s and (B) tan δ versus temperature. Different letters (A−D or a−b) in the same figure indicate significant differences (p < 0.05).

Figure 3. (A) Storage modulus (G′) and loss modulus (G″) of single-network gluten gels (SNGGs) and double-network gluten gels (DNGGs) versus different ratios of Fe3+ and PACs at a constant frequency of 10 rad/s and (B) tan δ versus ratio of Fe3+ and PACs. Different letters (A−E or a−e) in the same figure indicate significant differences (p < 0.05). and then fixed with 2.5% (v/v) glutaraldehyde in a 0.1 M phosphate buffer solution (pH 6.8), dehydrated using a series of alcohol solutions with increasing ethanol concentrations of 50, 70, 90 and 100% (v/v), and then dried with a CO2 critical point dryer (Tousimis Automatic, Rockville, MD, U.S.A.). The samples were then mounted on aluminum stubs and sputter-coated with a Baltek platinum coater. The internal microstructure of the hydrogels was observed using a scanning electron microscope (JEOL 6610, Tokyo, Japan) at an acceleration voltage of 10 kV. 2.6. Ultraviolet−Visible (UV−Vis) Spectroscopy Measurements. The abundance of the mono-, bis-, and tris-catechol−Fe3+/ PAC as a function of pH (2, 4, 6, 8, 10, and 12) was determined using an UV−vis spectrophotometer (TU-1810, Purkinje General Instrument Co., Ltd., Beijing, China) from 350 to 800 nm with a quartz cell having a path length of 1 cm. The stock solutions were diluted to 0.001% (w/v) and filtered using 450 nm syringe filters. The absorbance of the FeCl3 and PAC mixtures (Fe3+/PAC = 1:4) before and after adding gluten was then recorded. 2.7. Isothermal Titration Calorimetry (ITC). An isothermal titration calorimeter (Auto-ITC200, Malvern, Inc., Malvern, U.K.) was used to measure the enthalpy changes resulting from titration of FeCl3 solution into PAC solution. Aliquots (10 μL) of FeCl3 solution were injected sequentially into a 1.48 mL titration cell initially containing PAC solution in phosphate buffer solution. Each injection lasted 20 s, and there was an interval of 300 s between successive

injections. The temperature of the solution in the titration cell was 30.0 °C at pH 6.0, and the solution was stirred at 315 revolutions/min throughout the experiments. 2.8. Statistical Analysis. All of the experiments were conducted in triplicate. The experimental data were subjected to statistical analysis using commercial software (SPSS 17.0, SPSS, Inc., Chicago, IL, U.S.A.). Duncan’s multiple range tests were also applied to determine the difference of means from analysis of variance (ANOVA) using a significance test level of 5% (p < 0.05).

3. RESULTS AND DISCUSSION 3.1. Rheological Properties of Double-Network Wheat Gluten Hydrogels. The viscoelastic properties of the gluten hydrogels were characterized using a dynamic shear rheometer. As shown in Figure 1, the storage modulus (G′) and loss modulus (G″) of the hydrogels gradually increased with frequency, with G′ higher than G″ over the entire experimental angular frequency, indicating they are all hydrogels with solid-like behavior, as reported previously.24 As FeCl3, PACs, and the mixture of FeCl3 and PACs were added to the gluten dispersions separately, G′ and G″ were higher than that of the pure gluten hydrogel, with G′ increasing faster than G″. The typical G′ value of double-network gluten 6510

DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

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Journal of Agricultural and Food Chemistry Scheme 1. Schematic Illustration of the Preparation and Mechanism of Double-Network Gluten Hydrogels

Figure 4. (A) Storage modulus (G′) and loss modulus (G″) of single-network gluten gels (SNGGs) and double-network gluten gels (DNGGs) versus different concentrations of Fe3+ and PACs at the Fe3+/PAC ratio of 1:4 at a constant frequency of 10 rad/s and (B) tan δ versus temperature concentrations of Fe3+ and PACs. Different letters (A−D or a−d) in the same figure indicate significant differences (p < 0.05).

strength first increased but then decreased as the incubation temperature was raised (Figure 2A). For the double-network gels, the gel strength remained fairly constant from 20 to 40 °C but then decreased at the highest temperature. This suggests that there was some weakening of the forces holding the molecules together in the gels at the higher temperatures. One possible reason for this phenomenon is a weakening of the hydrogen bonding, because this type of interaction is known to decrease in strength as the temperature is raised. There was not a large impact of the incubation temperature on the phase angle of the gels (Figure 2B), with the tan δ values all being around 0.5, which indicates that the gels were predominantly elastic-like rather than fluid-like. 3.1.2. Effect of the Ratio of Fe3+ and PACs on the Gel Strength. Figure 3 and Figure S2 of the Supporting Information show the impact of the Fe3+/PAC molar ratio (RM) on the mechanical properties of hydrogels incubated at 40 °C for 30 min. The shear modulus of all of the doublenetwork gels was greater than that of the single-network gels

gels was about 1.5 kPa, which was 3 times higher than that of pure gluten hydrogel (500 Pa) at an angular frequency of 3 rad/s. These results suggested that the interaction of FeCl3 and PACs could improve the mechanical properties of gluten gels, leading to systems with high strength and toughness. Similarly, Liu and co-workers have reported that the addition of oligomeric procyanidins improves the viscoelasticity of wheat gluten.25 In the following experiments, the effects of the incubation temperature, ratio of Fe3+/PAC, Fe3+ concentration, and pH on the mechanical properties of the gluten hydrogels were systematically studied. 3.1.1. Effect of the Incubation Temperature on the Gel Strength. The frequency sweep data for hydrogels held at various incubation temperatures are shown in Figure 2 and Figure S1 of the Supporting Information. In general, the strength of the double-network gels was greater than that of the single-network gels across the whole range of temperatures studied (Figure 2A). For the single-network gels, the gel 6511

DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

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Journal of Agricultural and Food Chemistry

Figure 5. (A) Storage modulus (G′) and loss modulus (G″) of single-network gluten gels (SNGGs) and double-network gluten gels (DNGGs) versus different pH values at a constant frequency of 10 rad/s and (B) tan δ ratio versus pH value. Different letters (A−D or a−e) in the same figure indicate significant differences (p < 0.05).

Figure 6. SEM images of (A) single-network gluten gels (SNGGs), (B) PAC-added single-network gluten gels, (C) Fe3+-added single-network gluten gels, and (D) double-network gluten gels (DNGGs).

hydrophobic regions on proteins, respectively.26 Moreover, the Fe3+ and catechol ligands of PACs can form a double network with gluten gels via hydrogen bonding and hydrophobic interactions (Scheme 1). The decrease in the gel strength observed at higher RM values may be a result of a change in the structure of the gels induced by the high level of cross-linking agents present. For instance, there may have been a collapse in the gel structure, which reduced the overall shear modulus. 3.1.3. Effect of the Fe3+ Content on the Gel Strength. The 3+ Fe content was also important in determining the gel strength of the double-network gluten gels (Figure 4A and Figure S3A of the Supporting Information). Interestingly, adding low levels of iron (0.125−0.5 mM) led to the formation of double-network gels that were weaker than the singlenetwork gels, but adding higher levels of iron (2 mM) led to stronger gels. The tan δ values of the double-network gels were

(Figure 3A). As expected, the gel strength of the doublenetwork gels depended upon the amount of iron and PACs incorporated into them. The G′ value of the double-network gels increased as RM was raised from 1:2 to 1:4 but then decreased when it was raised higher. The phase angle of the gels was not strongly impacted by the level of iron and PACs present, being around 0.47−0.55° for all samples (Figure 3B), which again indicates that they were all predominantly elastic materials. These results suggest that the mechanical properties of the hydrogels can be tuned by varying the level of Fe3+ and PACs present. The increase in the gel strength with RM can be attributed to an increase in the number and/or strength of the interactions between the constituents within the gels. Previous studies have reported that the phenolic hydroxyl groups and hydrophobic regions on PACs can react with the carbonyl groups and 6512

DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

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Journal of Agricultural and Food Chemistry

Figure 7. UV−vis absorption profiles of Fe3+ and PAC solutions with a Fe3+ concentration of 0.5 mM and a PAC concentration of 2 mM at different pH in the (A) absence and (C) presence of gluten protein. (B) Samples were yellowish at pH 2, blue at pH 4 and 6, and red at pH >8.

In summary, these results suggest that the strongest doublenetwork gels can be formed for systems containing 0.5 mM Fe3+ and 2 mM PACs (RM = 1:4) at pH 6.0. 3.2. Microstructure of the Double-Network Hydrogels. Scanning electron microscopy (SEM) was used to observe the morphology of the surfaces of freeze-dried gluten hydrogels. The SEM images showed that all of the hydrogels had highly porous surfaces with cavities that varied in dimensions from a few micrometers to a few tens of micrometers (Figure 6A). The addition of Fe3+ or PACs did not have a major impact on the overall microstructure of the gels, which suggests that they may simply have increased the number and/or strength of the cross-links between structural entities that were already in contact. Similarly, it has been reported that the catechol side chain of dopamine methacrylamide formed a tris complex with Fe3+ ions, thereby increasing the local cross-linking density.28 Moreover, it has been reported that hyaluronic acid−calcium phosphate hydrogels containing calcium phosphate had a highly porous structure with interconnected pores, implying that the network structure of the hydrogels was maintained after the in situ cross-linking process.29

slightly higher than those of the single-network gels (Figure 4B), but the Fe3+ level present did not have a major impact on their phase angle. 3.1.4. Effect of pH on the Gel Strength. The impact of pH on the mechanical properties of the double-network gels was characterized using dynamic shear rheology measurments at 25 °C (Figure 5 and Figure S4 of the Supporting Information). Under highly acidic conditions (pH 0.8−2.0), the gels had relatively low G′ values, which were close to those observed for the single-network hydrogels. In contrast, at pH 6.0, the double-network gels had much higher G′ values (>2.5 kPa), which suggests that cross-linking was promoted under these conditions. Earlier studies have reported that monocatechol− Fe3+ complexes are formed between iron and 3,4-dihydroxyphenylalanine (DOPA) at low pH values, but bis- and triscatechol−Fe3+ complexes are formed at higher pH values.27 Consequently, one might have expected more cross-linking of the proteins at higher pH values. There was, however, an appreciable decrease in the G′ values of the double-network gels under alkaline conditions, which may have been due to changes in the solubility characteristics of gluten or iron. Iron is known to be much more soluble under acidic conditions than under alkaline conditions. 6513

DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

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Journal of Agricultural and Food Chemistry 3.3. Reinforcing Mechanism of Double-Network Gluten Gels. 3.3.1. UV−Vis Spectroscopy. The impact of pH on the self-assembly of Fe3+ and PACs in gluten hydrogels was characterized using UV−vis spectroscopy. The UV−vis spectra of Fe3+ and PAC coordinated solutions are shown in Figure 7A. No absorption peaks were observed for the pure Fe3+ or pure PAC solutions across the whole visible region (390−780 nm). Similarly, no absorption peaks were observed for the Fe3+−PAC solutions under acidic conditions (pH 2 or 4). Conversely, an absorbance peak was observed in the spectra obtained for the Fe3+−PAC solutions from pH 4 to 12. The maximum of this peak occurred within the range from 540 to 491 nm. This change in the absorption spectra with pH was related to the visible change in the appearance of the samples. The samples were yellowish at pH 2, blue at pH 4 and 6, and red at pH >8 (Figure 7B). Previous studies have reported that the coordination of Fe3+ and tannic acid is pH-dependent. There is a pH-induced transition between mono, bis, and tris complexes in catechol−Fe3+ polymer networks.20 The absorbance peaks observed at 550 and 495 nm at the higher pH values are indicative of the formation of bis and tris complexes, respectively. The UV spectra of Fe3+ and PAC coordinated solutions containing gluten were also measured (Figure 7C). These mixtures had similar UV−vis absorption spectra as the Fe3+ and PAC coordinated solutions. This result suggests that the properties of the double-network gels were influenced by Fe3+−PAC coordination at different pH values. 3.3.2. ITC. ITC was used to provide further insights into the interactions between Fe3+ and PACs (temperature of 40 °C and pH 6.0). The ITC profile obtained when 20 μM Fe3+ solution was titrated into 200 μM PAC solution is shown in Figure 8A. The peaks resulting from each injection were endothermic and decreased in magnitude as the number of injections increased. This result suggests that there was an interaction between PACs and Fe3+, which was presumably due to binding of iron ions to polyphenol molecules. The observed decrease in magnitude may therefore be due to progressive saturation of the binding sites on PACs. Thus, for the later injections, there are fewer binding sites available for the iron ions to bind. The binding enthalpy (ΔH) was calculated from the heat flow profile data by extrapolating the fitted curves to zero molecular ratio. The experimental titration data were then fit using a one-set-of-sites model, and the values for the number of binding sites (N), binding constant (KD), and enthalpy change (ΔH) were calculated (Figure 8B). The parameters that gave the best fit between the model and experimental data were N = 0.26, KD = 25 × 10−9 M, and ΔH = 1.3 kcal/mol, which suggest that the binding was relatively strong. The binding site parameter suggests that a single iron ion bound to about four PAC molecules and presumably linked them together, thereby increasing the mechanical strength of the gluten gels. Previous researchers have reported that catechol and Fe3+ ions can undergo pH-induced transitions between mono, bis, and tris complexes in metal−phenolic networks.30 3.4. Self-Healing Behavior. The self-healing ability of the double-network gels prepared at various pH values was evaluated using repeated compression−decompression rheological analysis (Figure 9). The G′ and G″ values of the hydrogels were determined when alternating strains of 1 and 1000% were applied. The G′ value went from a high value at 1% strain to a low value at 1000% strain, which suggested that

Figure 8. (A) Raw thermogram trace from an experiment of a FeCl3− PAC interaction, titrating 10 μM FeCl3 injections into the calorimetry cell of PAC solution. A weak constant heat of dilution can be discerned. (B) Corresponding plot after integration of peak areas and normalization to yield a plot of molar enthalpy change against the FeCl3/PAC ratio. DP represents the corrected heat rate.

there was some disruption of the gel network at high applied deformations. However, the G′ values recovered to values that were fairly close to the values measured during the first cycle, after multiple compression−decompression cycles were applied. This suggests that the hydrogels had good self-healing properties. Our results are consistent with previous studies that have shown that gluten gels have self-healing properties.31 Similarly, G′ of alginate-2-hydroxypropyltrimethylammonium chloride chitosan hydrogels immediately recovered once the strain was removed, regardless of the loading period.32 In conclusion, in this work, double-network gluten gels were fabricated by cross-linking of gluten using in situ coordination of Fe3+ and PACs. This approach led to gluten hydrogels with stronger and tougher mechanical properties once the fabrication conditions were optimized: 0.5 mM Fe3+ and 2 mM PACs (pH 6.0). The double-network gels had good selfhealing properties, meaning that they could recover their rheological properties after a large-scale compression− decompression cycle. The formation of a coordination bond between Fe3+ and PAC molecules likely explains the good mechanical properties observed in double-network gels. The hydrogel fabrication method used is simple and can be performed using inexpensive food-grade ingredients, which makes it a commercially viable method. 6514

DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

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Journal of Agricultural and Food Chemistry

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gels (SNGGs) and double-network gluten gels (DNGGs) with different pH values (Figure S4) (PDF)

AUTHOR INFORMATION

Corresponding Author

*Telephone: +86-532-88030448. E-mail: [email protected]. ORCID

David Julian McClements: 0000-0002-9016-1291 Qingjie Sun: 0000-0002-7371-1052 Funding

This work was supported by the National Natural Science Foundation of China (Grant 31671814) and the Special Funds for Taishan Scholars Project of Shandong Province, China (ts201712805). Notes

The authors declare no competing financial interest.

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Figure 9. (A) Storage modulus (G′) and loss modulus (G″) of singlenetwork gluten gels (SNGGs) and double-network gluten gels (DNGGs) versus number of cycles and (B) storage modulus (G′) (solid symbols) and loss modulus (G″) (hollow symbols) of singlenetwork gluten gels (SNGGs) and double-network gluten gels (DNGGs) when the Fe3+/PAC ratio was 1:4, the Fe3+ content was 2 mM, and the alternate step strain switched from small strain (γ = 1.0%) to large strain (γ = 1000%) at a fixed angular frequency (10 rad s−1). Each strain interval was kept as 100 s.

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REFERENCES

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.9b01649. (A) Frequency dependence of storage modulus (G′) (solid symbols) and loss modulus (G″) (hollow symbols) and (B) tan δ of single-network gluten gels (SNGGs) and double-network gluten gels (DNGGs) with different incubation temperatures (Figure S1), (A) frequency dependence of storage modulus (G′) (solid symbols) and loss modulus (G″) (hollow symbols) and (B) tan δ of single-network gluten gels (SNGGs) and double-network gluten gels (DNGGs) with different ratios of Fe3+ and PACs (Figure S2), (A) frequency dependence of storage modulus (G′) (solid symbols) and loss modulus (G″) (hollow symbols) and (B) tan δ of double-network gluten gels with different concentrations of Fe3+ and PACs at the Fe3+/PAC ratio of 1:4 (Figure S3), and (A) frequency dependence of storage modulus (G′) (solid symbols) and loss modulus (G″) (hollow symbols) and (B) tan δ of single-network gluten 6515

DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516

Article

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DOI: 10.1021/acs.jafc.9b01649 J. Agric. Food Chem. 2019, 67, 6508−6516