Enzymatic nanocomposites with the radio-frequency field modulated

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Enzymatic nanocomposites with the radio-frequency field modulated activity Yulia I Andreeva, Andrey S. Drozdov, David Avnir, and Vladimir V. Vinogradov ACS Biomater. Sci. Eng., Just Accepted Manuscript • DOI: 10.1021/acsbiomaterials.8b00838 • Publication Date (Web): 30 Oct 2018 Downloaded from http://pubs.acs.org on October 30, 2018

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ACS Biomaterials Science & Engineering

Enzymatic nanocomposites with radio-frequency field modulated activity Yulia I. Andreeva,† Andrey S. Drozdov,∗,† David Avnir,‡ and Vladimir V. Vinogradov∗,† †Laboratory of Solution Chemistry of Advanced Materials and Technologies, ITMO University, St. Petersburg, 197101, Russian Federation ‡Institute of Chemistry and the Center for Nanoscience and Nanotechnology, the Hebrew University of Jerusalem, Jerusalem, 91904, Israel E-mail: [email protected]; [email protected]

Abstract The control over enzymatic activity by physical stimuli is of interest to many applications in medicine, biotechnology, synthetic biology, and nanobionics. While the main focus has been on optically-responsive systems, alternative strategies to modulate the enzymatic activity of hybrid systems are needed. Here we describe a radiofrequency (RF) field controlled catalytic activity of an enzymatic sol-gel composite. For instance, the activity of bovine carbonic anhydrase entrapped in sol-gel derived magnetite (enzyme@ferria) composite was accelerated by a factor of 460% compared to its initial value, by applying the RF field of 937 A/m, with fast response time. This acceleration is reversible and its magnitude controllable. An acceleration mechanism, based on RFinduced heating of the magnetite by the Néel relaxation effect, is proposed and proven. The entrapment within a sol-gel matrix solves the problem of enhancing activity by heating without denaturing the enzyme. RF-controlled enzymatic composites can be

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potentially applied as biological RF-sensors or to control biochemical reactions within living organisms.

Keywords enzymatic nanocomposites; enzymatic activity modulation; electromagnetic field; stimulicontrolled biocomposite; sol-gel.

Stimuli-responsive enzyme-material composites are of central interest for a wide variety of biomedical and biotechnological needs. The enzymatic activity of such materials typically is modulated by external stimuli which are of chemical in nature - such as varying the pH, 1,2 introducing specific ions 3,4 or co-factor molecules. 5,6 Alternatively, it can be physical in nature such as varying the temperature 7,8 or triggering/modulating with a variety of irradiations, including ultrasount, 9 light, 10,11 electric fields, 12–14 or magnetic fields. 15,16 The application of radio frequency (RF) emission for modulating enzymatic activity - the focus of this report - is attractive due to its excellent penetrability which still leaves tissues unharmed, and yet compared with the other stimuli listed above, research on RF applications has been much less explored. Examples include enzymes entrapped in a thermoresponsive polymeric gel doped with Fe2 O3 nanoparticles (NPs), where an RF field was used to change the polymer conformation, allowing the enzyme to interact with substrate; 17,18 the entrapment of enzymes within a polymeric matrix with magnetic rods, such that low-frequency caused them to vibrate, increasing the mass transfer within the polymer; 19 enzymes immobilized in chitosan beads with magnetic NPs, allowing a rotating magnetic field to increase the reaction rate due to the induced magnetic stirring; 20,21 changing the enzymatic reaction rate by applying a nonheating magnetic field on magnetic nanosuspensions; 22,23 and the activation of a thermophilic enzymes by applying an alternating magnetic field. 24,25 In this article, we present the first 2


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example of an activity enchantment of a non-thermopilic enzyme, carbonic anhydrase, under the influence of RF-field. The observed effect was achieved through the entrapment of enzymes within magnetite sol-gel matrix and was the combined result of two phenomena: the heating of magnetite nanoparticles under the influence of RF-fields by the Néel relaxation effect, 26 and the high thermal stability of the enzymes entrapped within sol-gel derived materials. 27–30 Upon the irradiation of this biocomposite by the RF field at a frequency of 210 kHz and amplitude of 937 A/m, the catalytic reaction rate was boosted up to 460% of its initial value in a fast and reversible manner. Specifically, we have selected carbonic anhydrase from bovine erythrocytes (CAB) for that study, one of the most efficient and well-studied and a member of an important class of enzymes used in Alzheimer disease treatment. 31

Figure 1: CAB@ferria nanocomposites structure. SEM image of the CAB@ferria particles (a); EDX mapping of the CAB@ferria particles, iron signal corresponds to magnetite, nitrogen signal corresponds to CAB (b); HR-SEM image of the CAB@ferria composite (c); TEM image of the CAB@ferria, the crystalline interspacing of magnetite is shown in the inset (d); XRD spectra of CAB@ferria (correlated to JCPDS No. 19-0629 showed as red lines) (e); Schematic representation of the entrapment of the enzyme within the interstitial porosity of the aggregated ferria. (f).

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Entrapment of enzymes in magnetite sol-gel materials - a long-standing challenge - became possible after the development of a stable magnetite sol (Ferria) with a mean particle diameter of 10 nm, free of any sol-stabilizing agents, and at a neutral pH. 32 The unique feature of the ferria is its high zeta potential (valued +31 mV at pH 7.0) ensuring the high colloidal stability under biocompatible conditions and capability to undergo sol-gel transition at the room temperature. 33 These features originate from the chemical properties and composition of the ferria NPs: due to special synthetic conditions the NPs surface is enriched by Fe(II)-OH groups, which, on one hand shift the isoelectric point of the NPs to higher pH values, and on the other, facilitate the formation of interparticle Fe-O-Fe bonds in a course of partial dehydration of the surface at the room temperature, leading to a mesoporous inorganic matrix formation (see ESI, Fig. S1). 32 The enzyme was entrapped within a magnetite sol-gel derived matrix, by a recent protocol we have developed, described in ref. 34. Buffered CAB solution was added to the ferria hydrosol with a subsequent water removal and sol-gel condensation process. The produced hybrid ceramic material was washed with buffer solution to remove any adsorbed enzyme molecules and grinded to obtain a composite mesoporous powder (grain size 5-7 µm, Fig 1a) designated as CAB@ferria (see ESI Materials and Methods section for the details). The composite material demonstrated a high degree of homogeneity with the uniform distribution of the components as it was seen from EDX analysis (Fig. 1b). The mesoporosity of the composite material gave rise to a nitrogen-accessible surface area of 120 m2 /g and average pore diameters of 8.2 nm, as calculated by the BET and BJH equations, respectively (ESI Fig. S2), with the enzyme, entrapped and buried within the material (fig. 1c-d). The elementary building blocks of the aggregated powder were highly crystalline magnetite NPs with a mean diameter of about 10 nm, as revealed by XRD and TEM. The XRD pattern of the ferria nanoparticles corresponded to the pattern of magnetite (JCPDS No. 19-0629) with the typical main peak at 35.45◦ attributed to the plane with Miller indices of (311) (Fig. 1e). Also, a typical 2.86 ˚ Acrystalline spacing of magnetite was seen on the HR-TEM image (Fig. 1d insert). 34 For composite materials with

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mass fractions of CAB below 10 % wt, full entrapment was observed, and enzyme release into buffer solutions was absent. While the physical entrapment of enzyme within sol-gel matrix prevents the leaching of the enzyme, it was still catalytically active, with in-diffusion of substrate molecules and out-diffusion of product molecules through the pore network (Fig. 1f).

Figure 2: (a) Kinetics of pNPP formation by CAB@ferria with and without the applied RF-field; (b) Catalytic activity of CAB@ferria with periods of irradiation and relaxation are 2 min. The experiments were carried out in thermostatic conditions. The activity of the CAB@ferria composite was evaluated by measuring the hydrolysis rate of p-nitrophenyl acetate (pNPA) to p-nitrophenol. In the absence of RF irradiation, the hydrolysis rate of pNPA at 37 ◦ C by was found to be 23 µmol/min per mg of the composite. In order to evaluate the effect of RF field on the enzymatic activity the biocomposite was placed inside an inductive RF coil, and the alternating magnetic field with a frequency of 210 kHz and field amplitude of 937 A/m was applied under thermostatic conditions at 37 ◦ C. Under the influence of RF field, a significant boost of the catalytic activity to 105 µmol/min was observed, which is 457 % increase of its original value (Fig. 2b). It can be seen from the kinetic curve that the reaction rate rapidly reach a steady mode and remains literally on the same level during the whole experiment. The reversibility of this acceleration was demonstrated by following the response to switching the RF field on and off in the following experiment: A cuvette with a buffered dispersion of the CAB@ferria particles was subjected to several cycles of RF-irradiation (210 kHz, 937 A/m) and relaxation periods of 2 minutes 5



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each. The catalytic activity of the CAB@ferria composite under the influence of RF-field (210 kHz, 937 A/m) was repeatedly enhanced to an average of 450 % of its initial rate while returning to its original value when the field was removed (Fig. 2c). For the interpretation of the observed phenomena, the influence of the RF-field on CAB@ferria is to be addressed. It is known, that magnetic materials are generating heat under the influence of high-frequency oscillating magnetic fields as a result of relaxation processes, which involves the gradual alignment of the magnetic moments during the magnetization process. These relaxation processes may mainly take place through two distinct mechanisms: the Brownian relaxation and the Néel relaxation, but for NPs with diameters around 10 nm (our case) the Néel mechanism is thought to be predominant. 35 In that case, heat is dissipated from the magnetic particles by the delay in the relaxation of the magnetic moment through the rotation within the particle, and can be given by the equation 1:

2 F = µ0 χ”f Happly

(1)

where P is the heat dissipation value, µ0 the permeability of free space, χ” the AC magnetic susceptibility (imaginary part), f the frequency of applied AC magnetic field and Happly the strength of applied AC magnetic field. This effect is frequently used for biomedical purposes for so-called magnetic hypothermia of cancer tissues. 36,37 In order to measure the heating effect of the RF field on CAB@ferria, the material was investigated with a heat imager (Fig. 3). Heat image of the irradiated material in air showed that the composite is heated up to 62 ◦ C under the influence of the RF field within the 1 minute of exposure (Fig. 3b). Further heating occurs at a much slower rate, and the temperature reached 64 ◦ C only after 16 minutes of irradiation (Fig. 3d). Although the measured temperature and the visualized heat images were taken from the surface of the sample, the temperature within the material should be on the same level due to the short relaxation time of the heat conduction within magnetite nanoparticles (≈10 ns), 38 resulting in homogeneous heating of the entrapped distributed enzyme molecules in the CAB@ferria composite. It should be 6


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noted that no change of the dispersing water temperature was detected during the whole experiment, due to the low volume (5*10−4 %) and mass (2*10−3 %) fractions of the magnetic material, and it was maintained at the level of 37 ◦ C. At the same time it is known that the temperature difference for the surface of magnetically-heated nanoparticles and the media can reach tremendous values (up to 70 ◦ C for 5 nm), 39 so it can be assumed that while the water temperature was remained at the same level, the CAB@ferria NPs was heated to the temperatures close to one measured on the air.

Figure 3: Temperature maps of CAB@magnetite subjected to RF fields: field is off (a); after 1 (b), 5 (c) and 16 (d) minutes of irradiation. The temperature was measured at M2 and HS1 marks in addition to the heat map. The next question to be answered is, how did the entrapped enzyme react to the temperature rise? In contrast to all the systems described earlier, the free CAB is known to have low thermal stability and readily denaturates at 68 ◦ C. 40 This fact is agrees with the experimental results of free CAB by dynamic scanning calorimetry (DSC) (Fig. 4a). In contrast, entrapment within the magnetite sol-gel matrix enhanced the thermal stability of CAB and shifted its denaturation temperature up to 97 ◦ C (!), as seen from the DSC curve (Fig. 4a). The origin of this stabilization comes from strong interactions of the enzyme molecules with the pores of the sol-gel derived matrix, and were described earlier for this kind of materials. 1,41,42 Due to the higher thermal stability entrapped CAB, it was capable 7



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of performing the enzymatic reactions at higher temperatures and even demonstrated an Arrhenius-like behavior on the broader temperature range compared with the free enzyme (Fig. 4b). pNPA hydrolysis rate by CAB@ferria was rising until it reached its maximum near 60 ◦ C (111 µmol*min−1 *mg−1 ), while for the free enzyme a significant drop of the activity after 40 ◦ C was observed. The experiments were carried out under thermostatic conditions with preliminary incubation at the experimental temperature, so that the rate of the reaction was constant during the whole experiment. Notable is that the catalytic activity of CAB@ferria at 60 ◦ C is close to the one measured under the influence of the RF field (111 and 105 µmol*min−1 *mg−1 correspondingly). This fact can be used as an indirect indicator of the irradiated composite temperature in water solution. It should be noted, that the rate of the reaction per mg of the enzyme is 45 folds lower for the entrapped CAB in comparison with the free enzyme (18 vs. 817 µmol*min−1 *mg−1 for entrapped and free CAB correspondingly). This difference can be attributed to diffusional limitations of the reaction carried out by the heterogeneous catalyst. The effective diffusion coefficient Def f of pNPA within sol-gel matrix was estimated to be 38 folds lower than in solution valued 1.8*10−7 and 7*10−6 cm2 *sec−1 respectively (See Supporting Information for calculations). To determine whether the reaction is controlled primarily by the diffusion of the substrate or by the catalytic ability of the immobilized enzyme the Damköhler number was evaluated using the equation 2:

Da =

Vmax Def f KM δ

(2)

where Vmax is the maximal reaction rate, Def f is the effective diffusion coefficient, δ is the effective thickness of the unstirred layer through which the substrate must diffuse and KM is Michaelis-Menten constant (Table 1, See Supporting information for full calculations). The Damköhler number is the dimensionless ratio of reaction velocity to transport velocity, determining whether diffusion rates or reaction rates are more ”important” for defining a steady-state chemical distribution over the length and time scales of interest. For Da1 the 8


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reaction rate is much greater than the diffusion rate distribution is said to be diffusion limited while when 1Da the diffusion occurs much faster than the reaction. 43 It is estimated that the described systems the criterion was calculated to be 6.7 that indicated that the catalytic process was affected but not controlled by diffusion limitations. (See Supporting information for full calculations).

Figure 4: DSC curves of CAB@ferria and free CAB (a); temperature-activity dependence of free CAB and CAB@ferria (b). All experiments were carried out at thermostatic conditions. In order to better understand the difference between free CAB and CAB@ferria composite kinetic parameters Vmax and KM were measured at 20 and 50 ◦ C, and the results are presented in Table 1 (Fig. S3). It was found that for both systems the kinetic parameters are temperature-dependent: both systems were stable in the selected temperature region and demonstrated the rise of Vmax with the temperature elevation. It can also be noted, that CAB@ferria composite showed approximately two folds higher value of KM and 1.5 folds greater Damköhler number, which means an increase in the contribution of diffusion limitations to the kinetics of the overall reaction as the reaction rate grows faster than the diffusion rates. Table 1: Kinetic parameters of the enzymatic systems. System KM , µmol/L Vmax , µmol/min/mg Damköhler number ◦ CAB, 20 C 14.93 1785 CAB, 50 ◦ C 30.3 5181 CAB@ferria, 20 ◦ C 38.46 153 6.7 CAB@ferria, 50 ◦ C 69.9 775 9.9

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In order to prove the authenticity of the RF field effect on the enzymatic activity, several control experiments were performed. First, the possible effect of the applied field - with an amplitude of 937 A/m on the activity of free CAB was measured in solution, with and without dispersed magnetite no acceleration of the reaction was observed under these conditions (see Fig.s S4, S5, Supplementary material). Second, CAB was entrapped within a non-magnetic matrix - alumina boehmite according to the procedure of ref. 26., and then subjected to the RF field under similar conditions again, showing no acceleration of the enzymatic activity (Fig. S6). Third, the importance of the 3D entrapment was demonstrated by comparing with adsorption of CAB on the surface of the magnetite particles: slight inactivation to 90% of the initial activity, 210 kHz, 937 A/m) was observed (Fig. S7), reflecting the lower thermal stability of adsorbed enzymes in contrast with entrapped one. 41 Fourth, if indeed we are witnessing here thermally induced RF acceleration combined with matrix protection from denaturation, then this observation should not be unique for a CAB. Indeed, for confirmation purposes of the CAB study, a potential RF induced acceleration was checked for acid phosphatase AcP@ferria: exposure to the same RF field (210 kHz, 937 A/m) led to acceleration of the reaction rate by a factor of 3, from 51 µmol/min to 157 µmol/min (ESI fig. S8). In summary, we described the new class of stimuli-responsive biocomposites, based on enzymes entrapped within sol-gel derived magnetite. We showed that enzymatic activity of the sol-gel composites could be enhanced under the influence of RF field in a fast and reversible manner as an outcome of the following effects: heating of the CAB@ferria composite by to Néel relaxation mechanism, and thermal stabilization of the enzyme entrapped within sol-gel derived magnetite. The proof-of-concept was demonstrated for CAB and AcP, but it can be expected that the same principle can be applied for other enzymes. RF-sensible enzymatic systems can be an attractive tool for creation of biochemical radio receivers, radio-controlled catalytic materials or on-demand operating biochemical systems. Due to the fact that the RF-generated heat is rapidly dissipating in water, acceleration of biochemical reactions can be unpaired from heating of the media, affecting only

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few nanometers of the surrounding area. In contrast with light radiation, RF-fields have better penetration in biological media and are not inclined to damage biological objects. Such systems can be potentially applied for the augmentation of living organisms such as a bacteria, cell or even an animal, and be applied to the control of biochemical processes. 44

Acknowledgements This work was supported by the Russian Science Foundation, grant No. 18-79-00266. The authors declare no conflict of interests.

Supporting Information Supporting information is available. Supporting information contains the Materials and Methods section, supporting calculations and additional figures related to materials characterization and enzymatic kinetic evaluation.

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10.1021/bi00514a012. (41) Drozdov, A. S.; Shapovalova, O. E.; Ivanovski, V.; Avnir, D.; Vinogradov, V. V. Chemistry of Materials 2016, 28, 2248–2253, DOI: 10.1021/acs.chemmater.6b00193. (42) Avnir, D.; Braun, S.; Lev, O.; Ottolenghi, M. Chemistry of Materials 1994, 6, 1605– 1614, DOI: 10.1021/cm00046a008. (43) Mears, D. E. Industrial & Engineering Chemistry Process Design and Development 1971, 10, 541–547, DOI: 10.1021/i260040a020. (44) Huang, H.; Delikanli, S.; Zeng, H.; Ferkey, D. M.; Pralle, A. Nature nanotechnology 2010, 5, 602, DOI: 10.1038/nnano.2010.125.

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For Table of Contents Use Only Enzymatic nanocomposites with radio-frequency field modulated activity Yulia I. Andreeva, Andrey S. Drozdov, David Avnir and Vladimir V. Vinogradov

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Enzymatic nanocomposites with the radio-frequency field modulated

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