Specific Ion Effects on Hydrogel

Article Cite This: J. Phys. Chem. B 2018, 122, 10062−10067

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Influence of Metal Ions on the Melting Temperature, Modulus, and Gelation Time of Gelatin Gels: Specific Ion Effects on Hydrogel Properties Amanda Andersen, Casper Jon Steenberg Ibsen, and Henrik Birkedal* Department of Chemistry, Interdisciplinary Nanoscience Center (iNANO), 140 Langelandsgade, DK-8000 Aarhus C, Denmark

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S Supporting Information *

ABSTRACT: The impact of ions on hydrogel strength is not well understood, in particular with regards to specific ion effects for cations. Herein, we find that divalent and monovalent cations in most cases reduce the modulus and melting temperature while increasing the gelation time of gelatin hydrogels. This behavior is in contrast to the wellknown stiffening effect of trivalent metals. The melting temperature, the logarithm of the gelation time, and the logarithm of the amplitude of the complex modulus were found to follow a power law dependence on ionic strength: kIx. The power law exponent, x, was found to be universal within the groups of monovalent and divalent cations. The prefactor k depended linearly on the ionic radius, which was used as a proxy for ion polarizability. The slope of this linear dependence was different for monovalent and divalent cations.

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INTRODUCTION Hydrogels form through network formation through covalent bonding,1,2 physical interactions,1,2 or coordination bonds.3−7 They are widely employed in many areas of chemistry, biology, and materials science. Yet, the impact of ions on hydrogel properties has not been widely investigated, in particular in relation to hydrogel stiffness, gelation kinetics, and gel-melting temperatures.8−10 For example, Jaspers et al. showed that the properties of ethylene glycol-functionalized polyisocyanide hydrogels changed strongly upon changing anions, thus demonstrating anion-specific ion effects on temperatureresponsive hydrogels;8 however, these authors found no cation ion-specific effects, with the exception of lithium, on gelation temperature and no effects on hydrogel mechanics. Herein, we quantitatively investigate the influence of divalent and monovalent cations on gelatin hydrogels and demonstrate important cation ion-specific effects prompted by previous qualitative observations from our lab.11 Gelatin gels are kept together by networks of partially refolded collagen molecules interacting through physical interactions. They have extensively been used for many purposes including crystal growth media,12 fibrous scaffolds for biomedical applications13 such as wound healing14,15 and bone-mimics,16 bioadhesive films,17,18 not to mention its role as a structural agent in culinary science.19 For all such applications, the material will be in close contact with all sorts of body fluids, which contain a variety of salts in relatively high concentrations;20 the ion-specific effect of these on the physical properties of the biomaterial is an important factor when considering gelatin (and other hydrogel materials) for biomedical use. Additionally, the knowledge of the specific © 2018 American Chemical Society

influence of metal ions on hydrogel properties can be incorporated in material design and modulation.3,7,21,22 Ions in aqueous media influence the properties of the mixture such as the activity of other species, the viscosity of the medium, and so on.23,24 In addition to the well-known saltingin and salting-out effects, specific ions also influence the properties of macromolecular systems. To name but a few examples,24 their impact includes effects on hydrogel swelling behavior,25,26 the lower critical solubility of NIPAM (Nisoprolyacrylamide)-based thermoresponsive copolymers,27,28 and the adsorption kinetics and surface rheological behavior of copolymers at air/solution interfaces.29,30 These specific-ion or Hofmeister effects have been widely explored for anions but for cations much less so: although the cross-linking effects of coordination by trivalent- and transition-metal ions have been explored for various uses,21,22,31,32 only a few systematic studies have been published on cation Hofmeister effects26,33−37 including over 60-year-old studies on gelatin.26,34−36 However, even if these studies were systematic in terms of the added metal ion salts, the gelatin concentration (even if mentioned to be critical for material response35) varied between studies of different physical parameters. Thus, a systematic study of physical parameters under constant conditions is necessary to clarify and relate the systematic influence of metal cations on different gelatin hydrogel properties. Here, we study the impact of a selection of divalent and monovalent cation chlorides on gelatin hydrogel complex moduli, melting temperature, and gelation times. We find Received: August 7, 2018 Revised: October 12, 2018 Published: October 12, 2018 10062

DOI: 10.1021/acs.jpcb.8b07658 J. Phys. Chem. B 2018, 122, 10062−10067

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The Journal of Physical Chemistry B significant specific-ion effects that can be rationalized through correlation of the observed behaviors with the ionic radii and polarizability of the added cations.

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EXPERIMENTAL SECTION Gel Preparation. Gels were prepared by dissolving porcine gelatin powder (250 g bloom, Sigma-Aldrich) in a hot (55 °C) metal chloride salt solution to a final gelatin concentration of 150 mg mL−1. Dynamic Oscillatory Rheology. The mechanical properties of the gels were probed on a Physica MCR 501 rheometer (Anton Paar) using a 20.0 mL freshly prepared gel in concentric-cylinder mode. The cell was equipped with an evaporation cap to limit any effects of drying throughout the experiments. Alternating melting and hardening experiments were performed in succession, for a total of two melting and hardening experiments per sample. Prior to all tests, the gels were completely reset by heating to 55 °C (which is well above the upper critical solution temperature of gelatin38,39) for 5 min. The melting experiments consisted of a premelt hardening period of 135 min at 25 °C after which the temperature was increased to 45 °C at a rate of 0.2 °C/min. Thereafter, the gel was reset at 55 °C for 5 min and hardening experiments were performed at 25 °C for 500 min by lowering the temperature in a jump from 55 to 25 °C. The temperature reached 25 °C within 5 min, which is shorter than the gelation time at 25 °C for all samples. Then, the sequence was repeated. A sketch of the experimental profile is provided in Figure S1. Throughout the experiments, the gels experienced an oscillating strain, γ0, of 1% with an angular frequency, ω, of 1 Hz, both within the linear viscoelastic range of the system. Mechanical properties were probed every 20 s. Fourier Transform Infrared Spectroscopy. Gels containing KCl, MgCl2, and CaCl2 at I = 0, 0.2, 1, and 2 were prepared in D2O as described above and transferred to closed wells (Ø = 8 mm) in a PDMS (polydimethylsiloxane) mold to harden for 12 h. The absorption of the gels from 650 to 4000 cm−1 was measured using an Agilent Cary 630 Fourier transform infrared (FTIR) spectrometer.

Figure 1. Results from rheology experiments on a gel loaded with 0.2 M CaCl2. Full and dotted lines represent the storage (G′) and loss (G″) moduli, respectively. (A) Melting experiment. The intersection of G′ and G″ is interpreted as the melting point, Tm, where response changes from being predominantly elastic to predominantly viscous, that is, from solid to liquid. (B) Hardening experiment. The intersection between G′ and G″ is used as a measure of the gelation time, tgel.

The overall gel stiffness decreased close to exponentially with concentration for all the mono- and divalent metal salts tested (see below for a quantitative relationship). This concentration-dependent softening behavior can be attributed to electrostatic screening weakening the noncovalent cross-link bonds of the collagen network. All divalent cations investigated displayed the same overall trend; a strongly increasing softening of the gel stiffness with increasing salt concentration. However, the data showed systematic ion-specific differences in the decay rates. Ion-specific decay rates were also observed for the monovalent metal salts. This effect on the mechanical properties cannot be explained solely by classical charge screening, as that would infer identical ionic strength dependencies for equivalently charged ions. For both mono and divalent ions, the effect was seen to scale with the polarizability of the cations; Cs+ and Ba2+, the most polarizable cations, had the largest effect, whereas Mg2+ and Na+, the least polarizable, had the smallest effect. Ca2+ deviated from the trend, as the data points fell on essentially the same line as Sr2+. Sr2+ and Ba2+ both produced turbid gels, which was found to be caused by precipitation of small amounts of (Sr/Ba)SO4, with sulfate originating from the gelatin (see Supporting Information Figure S2). The loss of free Sr2+/Ba2+ because of precipitation was estimated to be at most 10 mM, which shifts the data points insignificantly and thus cannot be the reason for the quasicoincidence of the calcium and strontium curves. However, we cannot exclude that the presence of colloidal precipitate influences the rheological properties as silica colloids have previously been shown to increase the viscosity of aqueous gelatin.40 Similar patterns emerged for the melting temperature (Figure 2B) and gelation time (Figure 2C). The melting points decreased with ionic strength for both mono and divalent metal chlorides, following the same ion-specific order as in the hardening experiment, with the exception of sodium chloride. When sodium was added, we saw effectively no change in the melting temperature, within the precision of the experiments. Zn2+ (orange data points) deviated from the general divalent ion trend; for ionic strengths below 1.5 M (concentration of 0.5 M), the melting point was actually higher than the salt-free gelatin control. Shifting the fitted line (see below) for zinc downwards to match the value of the control experiment at zero ionic strength showed that it falls

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RESULTS We used dynamic oscillatory rheology to investigate the impact of added ions on the properties of hydrogel materials. Figure 1 shows an example of a melting (Figure 1A) and isothermal gelation (Figure 1B) experiment. Upon heating a hydrogel, for which the storage modulus G′ is larger than the loss modulus G″, the melting event, Tm, is seen as the temperature where the storage and loss moduli become equal. Conversely, the gelation time, tgel, can be determined as the time it took for the storage modulus to become larger than the loss modulus, Figure 1B. As a measure of gel materials’ properties, the gel stiffness, we used the amplitude of the complex modulus after a constant time (500 min). Figure 2 displays the logarithm to the gel stiffness (panel A), the melting temperature (panel B), and gelation time (panel C) as a function of ionic strength for a range of divalent and monovalent metal chloride salts. The divalent cations included the group II metals Mg2+, Ca2+, Sr2+, Ba2+, and the transition metals Mn2+ and Zn2+, whereas the monovalent cations were Na+, K+, Rb+, and Cs+. These were chosen because they span a wide range of ion polarizability. 10063


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Figure 2. Physical parameters extracted from rheology experiments as a function of ionic strength. Full symbols and open symbols in the same color correspond to divalent and monovalent cations from the same period of the periodic table, respectively. Lines are fits to data (see text); (A) logarithm of the stiffness of the gel after 500 min of hardening. All the monovalent and divalent metals soften the gels, the divalent more than the monovalent. The ability to soften the gels increased downwards within a main group, following the chaotropic Hofmeister series. (B) The melting points. With increasing ionic strength, the melting point was lowered exponentially by the divalent ions, whereas the monovalent ions tended to cause a linear lowering. The rate with which the melting point decreased was ion-specific. Zinc (orange data points) stands out as it induced a net increase of the melting point but otherwise followed the general trend as the other divalent metal ions. This is emphasized by the short dashed line showing the same curve shifted downwards for better comparison. (C) Gelation time as a function of ionic strength. The gelation time increased with salt concentration in an ion-specific way. Again, the qualitative behavior differed depending on the charge of the metal ion. The monovalent ions followed a close to linear dependence on the ionic strength, whereas the divalent ions did not.

Figure 3. Specific decay values, k, for gel strength (A), melting point (B), and gelation time (C) as a function of the ionic radius cubed (serves as a proxy for the ion polarizability). The straight lines are linear fits for the mono- and divalent ions, respectively.

were fitted to simple models for each of the metals. The fits are shown in Figure 2, divalent metals with full lines and monovalent metals with dashed lines. For all metal ions, the logarithm of the gel stiffness (Figure 2A) was found to follow the function

qualitatively in between Sr2+ and Cs+ (orange dashed line of Figure 2B). The stabilizing behavior can likely be attributed to the borderline metal nature of Zn2+ that allows it to form complexes with both carboxylic and amino groups41 as has been observed for trivalent ions,21,32,42 although it is not as clearly reflected in either the gel stiffness or the gelation time. Cu2+ shares many properties with Zn2+ and was therefore investigated for comparison, but quantitative experiments were abandoned because the ions reduced to solid Cu metal during experiments. Visual inspection did, however, show that the melting point was lowered like with the other divalent ions. The gelation time increased with ionic strength, displaying the same ion-specific ordering as the stiffness, that is, Ba2+ > Sr2+/ Ca2+ > Zn2+ > Mn2+ > Mg2+ for the divalent ions and Cs+ > Rb+ > K+ > Na+ for the monovalent ones, which is consistent with the chaotropic Hofmeister series.43 To obtain further insight into the observed behavior, the dependences on ionic strength for the three physical properties

log(|G*|500 (I )) = log(|G*0 |500 ) − kG *·I x ,

x≥1 (1)

where I is the ionic strength, |G* |500 is the gel stiffness at zero salt concentration, and k is an ion-specific decay constant. Similarly, the melting points (Figure 2B) and gelation time (Figure 2C) could be described by the functions 0

Tm(I ) = Tm0 − k Tm·I x ,

x≥1

0 log(tgel(I )) = log(tgel ) + k tgel·I x ,

(2)

x≥1

(3)

where again kTm and ktgel are ion-specific decay concentrations. 10064


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Figure 4. Infrared absorption of gelatin gels. (A) Amide I peak of gelatin gels containing CaCl2 at ionic strengths of 0, 0.2, 1, and 2 M. (B) Relative contribution of denaturated and helical collagen to amide I peak in gelation gels containing l, MgCl2 and CaCl2 at increasing ionic strength.

The decay constants found from the fits for gel strength, melting point, and gelation time as a function of the ionic radii cubed are shown in Figure 3A−C. The ionic radii used correspond to octahedral coordination (Mn2+ tetrahedral);44 the ionic radius cubed was used as a proxy for the ionic polarizability, which is reasonable for spherical ions.45 As a comparison, the data are also shown against computed polarizabilities for aqueous alkaline and alkaline earth metal ions in Figure S3 (values taken from Ninham et al.).46 Both instances revealed distinctly different linear correlations depending on cationic charge. Hofmeister effects have previously been shown to correlate with polarizability in other systems as well as depend strongly on ionic charge.46,47 The exponents from eqs 1−3 were found empirically to depend on the cation valence and not significantly on ionic radius, Figure S4. For monovalent ions, it was found to be close to 1.0 for the melting point and gel strength and averaging to 1.4 for the gelation time. For the divalent ions, it was found to be larger than one, averaging 1.4, 2.1, and 1.7 for the gel strength, gelation time, and melting point, respectively. For the latter two, the values seem to approximate the cation charge. For the former, the value is close to 4/3, which corresponds to the number-averaged charge of ions in the solution. The overall gel strength seems to be less sensitive to electrostatic screening, probably because it encompasses contributions from both entanglement and hydrogen bonding. To probe the structural change upon addition of metal ions, the infrared absorption spectra of the gels were measured. The amide I peak at 1720−1600 cm−1 was deconvoluted using a Gaussian band profile, assuming five Gaussian contributions, as described in literature.48−50 We found the two major contributions to the signal to be from helical collagen (∼1660 cm−1) and denaturated collagen (∼1630 cm−1).48−50 Figure 4A shows a zoom of the amide I peak in spectra of gelatin in CaCl2 solutions of ionic strength 0, 0.2, 1, and 2. As seen, the relative contributions to the peak shift toward lower wavenumbers as the ionic strength increases. This in good agreement with what has previously been shown for denaturation of collagen helices48−51 and reflects an increase in the ratio of denatured to helical collagen because of ioninduced destabilization of helical collagen. Figure 4B shows the ratio of the peak area corresponding to denaturated and helical collagen at increasing ionic strength for KCl, MgCl2, and CaCl2; the ratio clearly increases with ionic strength, with the smallest effect for KCl and the biggest for CaCl2. The full FTIR

spectra of gelatin gels with Ca2+, Mg2+, and K+ at ionic strengths of 0 and 2 are shown in Figure S5.

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DISCUSSION We found that divalent and, to a lesser degree, monovalent cations lead to drastic changes in gelatin hydrogel properties here characterized by melting temperature, gelation time, and the amplitude of the complex modulus. The observed destabilization of the gelatin network followed the series Ba2+ > Sr2+/Ca2+ > Zn2+ > Mn2+ > Mg2+ for divalent ions and Cs+ > Rb+ > Cs+ > Na+ for the monovalent ones, consistent with the chaotropic Hofmeister series. The chaotropic ions are known to destabilize, that is, salting in, many proteins at high ionic strengths, above 100 mMan effect which is often reversed between 10 and 100 mM ionic strength.43,52 In our study, all monovalent and divalent cations, with the single exception of Zn2+, destabilized the gelatin network over the entire concentration range. Although Zn2+ and Mn2+ were the only transition metals included in the quantitative study, qualitative observations indicated that Cu2+ also weakened the gelatin gels. In contrast to Mn2+, the Zn2+-loaded gels displayed atypical behavior with respect to the melting point, which was higher than the salt-free control up to a threshold concentration of 0.50 M Zn2+. We suggest that this is due to zinc binding to specific gelatin constituents forming strong cross-links, as is the case for trivalent ions.21,32 Zinc is a wellknown ligand in protein chemistry53 and has been used to form coordination cross-link-strengthened protein materials in marine worm jaws.54−59 Its complex cross-linking capability has been demonstrated in the literature using collagen analogues where it has also been shown to be reversible.60−62 The dependencies on ionic strength were found to adhere to power laws with a characteristic exponent common to all ions for a given property and cationic charge. This strongly suggests that this relationship is somehow universal for gelation hydrogels and thereby reflects the underlying physics of formation of these. For the monovalent cations, the power law reduced to a simpler linear dependency on ionic strength. We speculate that this results from the monovalent ions predominantly screening electrostatic repulsion between gelatin molecules. The divalent cations, in contrast, displayed more complex though still universal behavior, strongly indicating that their effects go beyond “simple” screening. Importantly, the observed reductions in gel stiffness, melting temperature, and increased gelation time could not be explained solely by electrostatic screening effects caused by 10065


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(2) Hoffman, A. S. Hydrogels for biomedical applications. Adv. Drug Delivery Rev. 2012, 64, 18−23. (3) Holten-Andersen, N.; Harrington, M. J.; Birkedal, H.; Lee, B. P.; Messersmith, P. B.; Lee, K. Y. C.; Waite, J. H. pH-induced metalligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 2651−2655. (4) Krogsgaard, M.; Behrens, M. A.; Pedersen, J. S.; Birkedal, H. Self-healing mussel-inspired multi-pH-responsive hydrogels. Biomacromolecules 2013, 14, 297−301. (5) Krogsgaard, M.; Andersen, A.; Birkedal, H. Gels and threads: mussel-inspired one-pot route to advanced responsive materials. Chem. Commun. 2014, 50, 13278−13281. (6) Krogsgaard, M.; Hansen, M. R.; Birkedal, H. Metals & polymers in the mix: fine-tuning the mechanical properties & color of selfhealing mussel-inspired hydrogels. J. Mater. Chem. B 2014, 2, 8292− 8297. (7) Krogsgaard, M.; Nue, V.; Birkedal, H. Mussel-inspired materials: Self-healing through coordination chemistry. Chem.Eur. J. 2016, 22, 844−857. (8) Jaspers, M.; Rowan, A. E.; Kouwer, P. H. J. Tuning hydrogel mechanics using the hofmeister effect. Adv. Funct. Mater. 2015, 25, 6503−6510. (9) Nebot, V. J.; Ojeda-Flores, J. J.; Smets, J.; Fernández-Prieto, S.; Escuder, B.; Miravet, J. F. Rational design of heat-set and specific-ionresponsive supramolecular hydrogels based on the hofmeister effect. Chem.Eur. J. 2014, 20, 14465−14472. (10) Swann, J. M. G.; Bras, W.; Topham, P. D.; Howse, J. R.; Ryan, A. J. Effect of the hofmeister anions upon the swelling of a selfassembled ph-responsive hydrogel. Langmuir 2010, 26, 10191− 10197. (11) Ibsen, C. J. S.; Mikladal, B. F.; Jensen, U. B.; Birkedal, H. Hierarchical tubular structures grown from the gel/liquid interface. Chem.Eur. J. 2014, 20, 16112−16120. (12) Kniep, R.; Busch, S. Biomimetic growth and self-assembly of fluorapatite aggregates by diffusion into denatured collagen matrices. Angew. Chem., Int. Ed. 1996, 35, 2624−2626. (13) Su, K.; Wang, C. Recent advances in the use of gelatin in biomedical research. Biotechnol. Lett. 2015, 37, 2139−2145. (14) Balakrishnan, B.; Mohanty, M.; Umashankar, P. R.; Jayakrishnan, A. Evaluation of an in situ forming hydrogel wound dressing based on oxidized alginate and gelatin. Biomaterials 2005, 26, 6335−6342. (15) Boateng, J. S.; Matthews, K. H.; Stevens, H. N. E.; Eccleston, G. M. Wound healing dressings and drug delivery systems: A review. J. Pharm. Sci. 2008, 97, 2892−2923. (16) Ko, C.-C.; Oyen, M.; Fallgatter, A. M.; Kim, J.-H.; Fricton, J.; Hu, W.-S. Mechanical properties and cytocompatibility of biomimetic hydroxyapatite-gelatin nanocomposites. J. Mater. Res. 2006, 21, 3090−3098. (17) Matsuda, S.; Iwata, H.; Se, N.; Ikada, Y. Bioadhesion of gelatin films crosslinked with glutaraldehyde. J. Biomed. Mater. Res. 1999, 45, 20−27. (18) Sung, H.-W.; Huang, D.-M.; Chang, W.-H.; Huang, R.-N.; Hsu, J.-C. Evaluation of gelatin hydrogel crosslinked with various crosslinking agents as bioadhesives:In vitro study. J. Biomed. Mater. Res. 1999, 46, 520−530. (19) Gómez-Guillén, M. C.; Giménez, B.; López-Caballero, M. E.; Montero, M. P. Functional and bioactive properties of collagen and gelatin from alternative sources: A review. Food Hydrocolloids 2011, 25, 1813−1827. (20) Reece, J. B.; Urry, L. A.; Cain, M. L.; Wasserman, S. A.; Minorsky, P. V.; Jackson, R. B. Campbell Biology; Pearson Education: Campbell, 2011; Vol. 9. (21) Baumbach, H. L.; Gausman, H. E. Aluminum and Chromium as Gelatin Hardeners. J. Soc. Motion Pict. Eng. 1946, 47, 22−54. (22) Covington, A. D. Modern tanning chemistry. Chem. Soc. Rev. 1997, 26, 111−126.

increased ionic strength. The systematic differences in prefactors, k, amongst cations correlated almost perfectly with the ion radius for all ions and with cation polarizability for the subset of ions for which such values were available. This further underlines the link between dispersion forces and specific ion effects23,24 and extends the previous studies on, for example, hydrogel swelling25 to include rheological parameters.

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CONCLUSIONS Specific-ion effects, or Hofmeister effects, are in themselves nothing new, but very little research has gone into the role of cations with respect to dispersion forces. In this work, we have investigated the impact of a broad range of cations on the hydrogel strength of gelatin gels. We have demonstrated that salt-induced disruption of a simple physically cross-linked hydrogel network goes beyond simple electrostatic screening in that the mechanical properties also depended on the specific choice of salt. The systematic differences were found to correlate strongly with the polarizability of the cation used in a manner that differed depending on whether it was monovalent or divalent. Clearly, changing the ionic environment can have dramatic effects on the performance of hydrogel materials. The results presented herein underline that understanding specific ion effects should not be neglected when designing materials for use in salt-rich environments, but also present new opportunities for tailoring materials’ properties.

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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.jpcb.8b07658. Graphic representation of rheological measurement profile; turbidity measurements of BaCl2 and SrCl2 solutions; decay values plotted against calculated cation polarizability and representation of fit-exponents correlated to ionic radii; full FTIR spectra of K-, Rb-, and Cacontaining samples at 0 and 2 M (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: +4522508475. ORCID

Henrik Birkedal: 0000-0002-4201-2179 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Uffe Bjørnholt Jensen for experimental contributions and discussions in the early stages of this project. We thank Mie Elholm Birkbak and Jan Skov Pedersen for SAXS investigations during the course of this work; these investigations turned out not to be relevant for the final interpretation of all data. We gratefully acknowledge funding from The Lundbeck Foundation and from the Human Frontiers Science Program (HFSP, award RGP0004/2010) and funding for a rheometer from the Carlsberg Foundation.

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Specific Ion Effects on Hydrogel

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