Ionic Liquids from Biocompatibility and Electrochemical Aspects

Nov 27, 2017 - Ionic Liquids from Biocompatibility and Electrochemical Aspects toward Applying in Biosensing Devices. The introduction of a novel ioni...
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Feature Cite This: Anal. Chem. 2018, 90, 640−648

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Ionic Liquids from Biocompatibility and Electrochemical Aspects toward Applying in Biosensing Devices The introduction of a novel ionic environment, which is composed of a large, asymmetric organic cation and inorganic (or organic) anion that loosely fit together, is extending the properties and classical applications of chemical/biochemical and industrial performances. In this Feature, we discuss the recent uses of ionic liquids in enzyme activation and their combination with nanosized materials and electrode structures to enhance the sensing performance of biobased sensing devices. Faezeh Ghorbanizamani† and Suna Timur*,†,‡ †

Ege University, Faculty of Science, Biochemistry Department, Bornova, Izmir, Turkey, 35100 Ege University, Central Research Testing and Analysis Laboratory Research and Application Center, Bornova, Izmir, Turkey, 35100 approximately 100 °C or below, which is an arbitrary temperature limit. A typical IL is largely composed of ions (large organic cation and small anion) and short-lived ion pairs. The difference in the sizes of the bulky cation and the small anion does not allow a lattice network to form, which occurs in many inorganic salts, and instead, the ions are disorganized. 13−15 As a result, ILs have a unique range of physicochemical properties, such as extremely low vapor pressure, a wide liquid range, low flammability, high electrical conductivity (between 0.1 and 20 mS cm−1), good solvent properties for a wide variety of organic, inorganic, and organometallic compounds, high thermal stability (ILs are thermally stable up to 450 °C), and a large electrochemical window (4.5−5.0 V) that make it possible to use them in several applications13−17 (Scheme 1a). Moreover, by finetuning the structure of ILs, these properties can be tailored to satisfy the specific application requirements.18−20,20a Besides biosensor is an analytical device that uses a living chemical and physical properties of ILs, their potential organism or biomolecules to detect the presence of target bioactivity has become so fascinating for biochemists and analytes, and this detection event is transduced to provide a medical researchers20b Possible pharmaceutical and medicinal measurable response, preferably one that can be simply applications of ILs as well as systems, strategies and methods converted to an electrical signal so that the result can be fed which are related with the usage of ILs for these biobased to an electronic device for signal processing, data storage, 1−3 studies are presented in Scheme 1b,c, respectively.21 In this The determination of compounds by a biosensor has etc. article, we will consider examples of the applications in which many advantages, such as high specificity, fast measurement, ILs play a fundamental role in important fields, such as the simplicity, low reagent usage, reusability of biological elements, stabilization and activation of biomolecules, modification of and online measurement. Each biosensor generally has the electrode materials, and modification of nanoparticles. following three basic components: (i) a recognition element (such as enzymes, antibodies, peptides, and aptamers), (ii) a IL-BASED ELECTROCHEMICAL-SENSING LAYER physical transducer (e.g., electrochemical, optical, piezoelectric, To form IL-based electrochemical-sensing layers, numerous and thermometric), and (iii) a signal processing device (lightstrategies have been applied. The most commonly used sensitive and/or electronic device).4−7 Despite all the efforts in methods include direct mixing, physical adsorption, electrothe field of biosensors, further research is still need to improve deposition, casting and rubbing, sol−gel encapsulation, layertheir performances and commercialization as well as miniaturby-layer (LbL), and a sandwich-type immunoassay. A brief ization for their practical and common uses. The most explanation of each of these methods is summarized below. commonly used method is to use additives during the Direct Mixing. The first report on the development of manufacturing process to either mediate the biochemical “Bucky gel” materials by grinding suspensions of high-purity reactions, stabilize the biomolecule activity, or modify the single-wall carbon nanotubes in imidazolium-based ILs was sensor selectivity.8 Among various compounds, ionic liquids given by Fukushima et al. in 2003.22 Since 2003, this technique (ILs) have attracted a great deal of attention in various fields, 8−11 has been widely utilized for the preparation of carbon ionic Paul Walden first defined including biocatalytic processes. ILs, and it is still acknowledged today.12 ILs are materials Published: November 27, 2017 composed of cations and anions with melting points that are ‡

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DOI: 10.1021/acs.analchem.7b03596 Anal. Chem. 2018, 90, 640−648

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Physical Adsorption. Preparation of immobilized ligand molecules by physical adsorption of an enzyme onto a solid support is presumably the easiest and simplest method. This method is based on nonspecific physical adsorption between protein molecules and the surface of the support electrode by means of hydrogen bonds, ionic and hydrophobic interactions, as well as van der Waals forces.24,26,27 The nature of the forces involved in noncovalent immobilization mean the process can be reversed by changing the conditions that influence the strength of the interactions (e.g., pH, temperature, ionic strength, or polarity of the solvent).28 Enzyme adsorption as an immobilization method is a mild and practical method that usually preserves the catalytic activity of the enzyme. Such methods are low cost, but they may suffer from problems, such as enzyme leakage from the matrix, depending on the conditions and the relatively weak interactions.28 By using ILs, these problems can be excluded, and the biosensor performance can be improved. Casting and Rubbing. One of the most practical methods for creating protein-based biosensors is the stabilization of biomolecules onto carbon nanotube (CNT)/IL-nanocomposite-modified films via a casting technique. Casting is a manufacturing process in which liquid materials are usually poured into a mold. In this case, the proteins are successfully stabilized at the CNTs/IL composite surface by means of a poly(vinyl alcohol) (PVA) film.29,30 In the rubbing method, a dark gel formed by grinding a certain amount of premixed biomolecule/CNTs with an IL into which can be coated on a smooth glass side, and then, the pretreated glassy carbon electrode (GCE) can be rubbed to mechanically attach the gel to the surface.31 Electrodeposition. Electrodeposition has been described as a film development process that consists of the formation of a metallic cladding on a base material (substrate) via the electrochemical reduction of metal ions from an electrolyte to attain favorable electrical and corrosion resistances, reduced wear, and friction, improved heat tolerance, and a heat resistant nature. Owing to their properties, such as negligible vapor pressure, nonflammability, and heat resistant nature, ILs are a superior media for electrodeposition of metals and semiconductors. The use of ILs results in the ability to electrodeposit metals that have previously been impossible to reduce in aqueous solutions (such as aluminum) and to engineer the redox chemistry and control the metal nucleation characteristics.32,33a For example, electrodeposition of gold nanoparticles (AuNPs) onto IL/CNT had been studied to design AuNP/IL/CNT nanocomposite based biosensors. The IL assembled on the CNT and AuNP could further accelerate the electron transfer between the enzyme and electrode, and this fact contributed to obtain improved sensing performance.33b Sol−Gel Biomolecule Encapsulation. The sol−gel encapsulation or entrapment method is a method to retain biomolecules in a semipermeable host membrane or in a network matrix, such as hydrogels and other polymeric materials, via noncovalent interactions.34 A sol−gel encapsulation method for IL-based biosensors consists of the synthesis of an IL-silica sol, which is then mixed with biomolecules to obtain a sensing layer.24,34 Usually, encapsulation occurs under mild conditions, and the 3D-structure and function of the biomolecules remain intact. Moreover, the penetration matrixes allow the transport of low-molecular weight compounds without leaking the entrapped enzymes.34

Scheme 1. (a) General Properties and Some Common Applications of ILs, (b) Some of Pharmaceutical and Medicinal Applications of ILs (API-IL, Active Pharmaceutical Ingredient-Ionic Liquid), and (c) Systems, Approaches, and Methods Related with the Application of ILs in Biotechnological and Medical Area. Reproduced from Egorova, K.S; Gordeev, E.G.; Ananikov, V. P. Chem. Rev. 2017, 117, 7132−7189 (ref 21). Copyright 2017 American Chemical Society

liquid electrodes (CILEs) by directly mixing a certain amount of graphite powder with ILs in an agate mortar.23,24 The resulting mixture can be used as a bare electroactive surface, substrate for electrodeposition of metal nanoparticles or even immobilization of biomolecules to construct electrochemical biosensors.25 641

DOI: 10.1021/acs.analchem.7b03596 Anal. Chem. 2018, 90, 640−648

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Analytical Chemistry Layer-by-Layer. A layer-by-layer (LbL) technique is based on the sequential deposition of multiple layers to attach the final protein/enzyme layer onto an electroactive surface via various interactions such as electrostatic, van der Waals, hydrogen bonding, and ionic interactions.24 The LbL method provides a low-priced technique to form layered structures with prerequisite thicknesses and layer sequences from a wide variety of compounds. The packing density of the components in LbL films is not high, and this is beneficial for material transport across and along the layers. These characteristics are attractive for the fabrication of biological, nanosized devices.35,36 For instance, a glucose biosensor has been developed by the LbL method on a GC electrode. The results showed that the presence of IL significantly affected the electron transfer efficiencies of the modified electrode toward the oxidation of glucose.35 Sandwich-Type Immunoassay. The sandwich-type method includes immobilization of the primary antibodies on a solid-state support, and the sandwich immunocomplex is between the primal antibodies and the labeled antibodies that create a signal (usually enzyme-labeled antibodies or nanoparticle-labeled antibodies). The antigen−antibody reaction causes variations in the electrochemical signals, but this change is usually relatively small. For the development of an electrochemical immunoassay, the signal amplification and noise reduction are remarkable.37 To provide a convenient pathway and electrode surface, ILs were successfully used. In this case, ILs play a crucial role in elevating the sensitivity of the imunosensor when used in the structure of some carbon-based electrodes.38,39

Scheme 2. Strategies for the Stabilization and Solubilization of Proteins into ILs. Reprinted with permission from Macmillan Publishers Ltd.: NAT. MATER., Armand, M.; Endres, F.; MacFarlane, D. R.; Ohno, H.; Scrosati B. Nat. Mater. 2009, 8, 621−629 (ref 33a). Copyright 2009

biomolecules in the presence of organic solvents or ILs. The immobilization of biomolecules could be performed by using both physical adsorption and covalent attachment techniques without needing the complex laboratory procedures. The commercial availability of many immobilized enzymes (e.g., Novozym 435, which is a Candida antarctica-derived lipase B attached on an acrylic resin) is due to from the noticeable advantages of use of solid supports as an immobilization platform. CNTs with large surfaces and distinct nanoscale sizes are interesting and promising carriers that are accredited with high biomolecule loading with a low mass-transfer resistance.41 The enzyme-CNT conjugates well disperse in ILs and show a high enzyme activity and stability to heat compared to their native structure in ILs.42 On the other hand, ILs have the ability to undergo a polymerization process and form polymerized ILs or poly(ionic liquid)s (PILs), which carry IL monomers in repeating units. IL based polymer membranes are obtained by using various approaches including polymerization of the components with the formation of polycations, polyanions, copolymers, and superior, double-ion structures, also blending with a neutral macromolecule, typically polyvinylidene fluoride (Figure 1). These architectures have a potential to be replaced with perfluorosulfonic-acid structures as fuel cell membranes.33

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ENZYME STABILIZATION AND ACTIVATION It is well-known that ILs have good compatibility with various biomolecules, and even whole cells can be activated using different ILs.14 Some IL properties, such as the water-related activity, polarity, viscosity, pH, ability to form hydrogen bonds, excipients, and impurities, can influence enzymatic activity as well as catalytic performances.40 Generally, the stabilization and activation methods of proteins/enzymes with ILs can be separated into three main groups, a common method is basically the direct dispersion of the enzymes in ILs. Some lipases are known to be effective in this kind of dispersion. The other group consists of enzyme immobilization (on a solid matrix, sol−gel, or cross-linked enzyme aggregate (CLEA)) via covalent or physical attachment to polyethylene glycol (PEG) and cleansing with propanol. Enzymes are more resistant to denaturation when these methods are used. A third, more sophisticated methodology is based on a relatively new concept which involves water-containing IL microemulsions, IL-coated enzymes, additive-containing ILs, and enzyme-compatible, ionic media designs. Addition of small amounts of water to ILs may strongly affect the protein solubility while retaining the properties of the selected IL. These techniques tend to minimize the denaturing effects of ILs on biomolecules (such as hydrogen bonding and anion nucleophilicity reduction). Scheme 2 shows various strategies to solubilize and stabilize proteins into ILs.33 Enzyme Modification via Immobilization on a Solid Support. One of the major obstacles to the applying of enzymes in industrial procedures is their fragile structures as well as insufficient stabilities under the harsh operational conditions. Enzyme immobilization on a solid support is an efficient strategy to enhance the lifetime of catalytic

Figure 1. Different pathways for preparation of polymerized ILs. Reprinted with permission from Macmillan Publishers Ltd.: NAT. MATER., Armand, M.; Endres, F.; MacFarlane, D. R.; Ohno, H.; Scrosati B. Nat. Mater. 2009, 8, 621−629 (ref 33a). Copyright 2009. 642

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and precipitation has many advantages, such as increasing the interfacial area, enhancing the solubility of the substrates (hydrophobic and hydrophilic), and monodispersal of the enzymes at a molecular level.66,67 Enzyme Modification by Poly(ethylene glycol) (PEG). The standard method for enzyme stabilization under denaturating conditions is through enzyme interactions with PEG via physical or covalent interactions. PEG is a polymer containing hydrophobic and hydrophilic properties, and thus, the modified enzymes can be dissolved in organic solvents and ILs.68,69 In biochemistry, the aims of the chemical modification of enzymes with PEG are a reduction in their immunoreactivity and immunogenicity and an increase in the plasma half-life of the modified enzymes.70,71 Because of the high affinity and good solubility of PEG in an IL environment, PEG-lipase in hydrophobic ILs has a higher enzyme activity than that of the free form. Furthermore, a remarkable increase in the enzyme enatioselectivity compared to that of the free lipase was achieved.71 The increase in the reaction rate was suggested to be due to better dispersion of the lipase-linked PEG complex in the ILs than that in the free lipase suspension. Immobilized lipase provides lubricity to these solvent systems.61,72,73 Enzyme Modification by Cleansing with n-Propanol. Silica-immobilized enzymes are stabilized by repeated cleansing with dry n-propanol. This is called the propanol rinsed enzyme preparation (PREP).74 The procedure is essentially an association of three different approaches: (i) precipitating enzymes with alcohols, (ii) drying the precipitate by cleansing with n-propanol, and (iii) using a high amount of salt during coprecipitation. PREP has been developed into a preparation called “Enzyme modification with n-propanol rinsing and precipitation” (EPRP).75,76 The EPRP involves removing water from the immobilized enzyme by cleansing it with n-propanol, and the propanol rinses rapidly eliminate the water associated with the protein and minimize the enzyme denaturation. To reduce the side effect of propanol cleansing, nonaqueous IL media have been used, and the enzymes prepared by the EPRP method exhibit excellent activity in nonaqueous IL media compared to those prepared by the traditional method.67,77 Solvent Environment Modification by Water-Containing IL Microemulsions. To enhance biosensor performance, modifying the solvent environment is one of the methods that can be used to improve enzyme compatibility. Some reports have described the use of water-containing IL microemulsions as a medium to dissolve different enzymes and proteins (e.g., the lipase enzyme from Candida antarctica).77 Microemulsions are basically water droplets stabilized in nonpolar solvents by a layer formation of surfactants and are optically clear and thermodynamically stable.61 Microemulsions have been used as hosts for proteins and enzymes to perform biocatalytic reactions in organic solvents.61 This approach showed some advantages, such as enzyme entrapment in tiny water domains, enzyme protection against unfavorable reactions, and stabilization and activation of enzymes. Interestingly, in the past decade, the number of studies on the formation water-in-IL microemulsions has increased the use of anionic or nonionic surfactants.78−81 Physical coating/entrapment into a matrix is a relatively ordinary and frugal method that results in relatively small deviations in the native enzyme structure and function. The insolubility of some ILs in water and organic solvents make them good candidates as encapsulating materials for biomolecule immobilization. In the presence of the IL, a protecting shield covers the biomolecule, preventing structural changes.

Besides, the polymerized ILs can be utilized as materials for enzyme immobilization and produce a nonaqueous, ionic microenvironment for enzyme immobilization.43,44 In addition to the polymerized IL microparticles, magnetic nanoparticlesupported ILs formed by IL-saline covalent bonding on magnetic silica particles can be used as a solid support for enzyme immobilization.45 Magnetic nanoparticle-supported ILconjugated enzymes have some advantages, such as improved enzyme loading and catalytic efficiency and recovery and reusability without losing activity compared with that of the native counterpart. Layered double hydrophobic clays (LDHCs) can be used as an enzyme immobilization matrix without covalent binding due to their advantages, such as unusual intercalation properties and high porosity, and they act as a host matrix with hydrophobic characteristics. However, LDHC structures suffer from poor conductivity. The use of ILs to form IL-functionalized LDHCs can compensate the poor conductivity of the LDHCs and allow them to serve as effective support matrixes that are suitable for protein immobilization with the potential to create a new generation of biosensors.46 As a solid support base, silicapolyaniline-IL hybrid systems have been successfully used in the fabrication of biosensors.47 Silica is ideally suited for enzyme immobilization, but it is electrically isolative with a low charge-transfer efficiency and substrate diffusion. Therefore, it is necessary to have a conducting, ramified network to allow electron transfer between the enzyme and electrode. In this case, polyaniline and ILs can be used as electron transducers to augment the signal production by the enzymes.48 Enzyme Modification by Sol−Gel Encapsulation. Sol− gel encapsulation requires adequate hydrolysis precursors (tetraalkoxysilanes) in aqueous solutions to produce soluble hydroxylated monomers, and the SiO2 matrix formation results from the cross-linking condensation that facilitates the biomolecule encapsulation.47 Some of the disadvantages observed in these methods are gel shrinking and pore collapse. Additionally, alcohol production during silicon alkoxide hydrolysis is another observed issue that limits the function of this method.49 To solve these drawbacks, various methods have been suggested, and among these methods, the use of ILs as additives can regulate the protein hydration, resulting in the increased activity and stability of the enzymes.50−55 ILs are believed to act as both a mold for the formation of a mesoporous matrix, which enhances mass transfer, and as a stabilizer to improve the activity of the immobilized biomolecules in the sol−gel process.56−58 Enzyme Modification by Cross-Linked Enzyme Aggregates (CLEAs). As the predecessor of career-free immobilization; CLEA is a very useful approach to activate and stabilize many crude enzymes. CLEAs can be created via the interactions of the glutaraldehyde and amino groups present on the protein surface, which are almost entirely composed of protein with just a small amount of the crosslinking agent.59−61 This method has some advantages, such as the ease of preparation and recycling, the enhanced enzyme activity, the good stability in organic solvents, and multienzyme-containing biocatalyst immobilization.62−65 Aggregation and precipitation are regularly induced by the inclusion salts, organic solvents, nonionic polymers, or acids to precipitate the enzyme as physical aggregates from the glutaraldehyde. The structure of the aggregates and the catalytic activity of the individual proteins are preserved by the cross-linking. The addition of ILs to induce the aggregation 643

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Analytical Chemistry Therefore, the sensitivity increased and the response time decreased due to this advantage, and the performance of the biosensor improved.82−86 The IL-coated enzymes also showed increased enantioselectivity that was accompanied by remarkable reaction rates in different resolution reactions.87−90 These results indicated that the intensified activity of the IL-coated enzymes may be due to the easier access of the substrate to the more porous IL-coated enzyme and the enzyme flexibility and conformational changes exposed by its noncovalent interactions (Some substrates showed a 500 to 1000-fold acceleration). One of the promising designs on the use of “Task-specific IL” bearing a functional vinyl group in the cationic constituent of the molecular structure as a polymerizable IL for the preparation of enzyme encapsulated polymeric microparticles (PIL-MP) was reported in a previous work.43 In that work, the resulted PIL-MPs were obtained via polymerization reaction a water-in-oil (W/O) emulsion as shown in Figure 2.43

Figure 3. Comparison of the mechanism of electrode reaction of a polar reactant at a traditional oil-based carbon paste electrode and ILcarbon paste electrode (ILCPE). Arched arrows indicate heterogeneous electron transfer, whereas straight arrows indicate transfer across the liquid/liquid interface. Reproduced from Silvester, D. S. Analyst 2011, 136, 4871−4882 (ref 15), with permission of The Royal Society of Chemistry.

the large electroactive area for electron transfer on the ILs. Moreover, IL-modified CPEs and CILEs show a high conductivity and sensitivity as well as an antifouling ability for electroanalysis, which make them suitable electrode alternatives for detecting biomolecules in biosensors.92,94−97 Carbon Nanotube (CNT)-IL Composites. CNTs are an important group of materials with unique properties, such as a high surface area, high electrical and thermal conductivities, and unparalleled strength, making them ideal for applications in electrochemical devices. CNTs can aid the electron-transferring reactions and can be used as a biomolecule immobilizer. For instance, protein immobilization can occur through covalent bond formation between the −COOH groups of the CNTs and the −NH2 groups of the proteins.24 Despite all these advantages, CNTs are heavily entangled with each other and form agglomerates due to their rope and bundle structures. By dispersing the CNTs in ILs via mechanical milling to form a thermally stable gel, three-dimensional (3D) networks of untangled CNTs have been achieved.98−101 This type of modification improves the sensitivity of detection and lowers the detection potential to minimize the effect of interferences for a number of analytes, such as chloramphenicol and βnicotinamide adenine dinucleotide (NADH),98,99,102,103 and it can also be used for the thermal stabilization of some enzymes, such as laccase,100 for direct protein electrochemistry101 and for enhancing the electrocatalytic activity of enzymes.104,105 Composite materials based on mono- and multilayered carbon nanotube-ILs have an extremely low capacitance and background current compared to that of graphite and mineral oilbased CPEs, which opens a promising route to fabricate a third generation of biosensors.31,106−111 Compared with CNTs, carbon nanofibers (CNFs) have intrinsic advantages such as lower cost mass production, better mechanical stability, easier surface functionalization, and more edge sites on the outer wall.24,112 IL entrapment in a CNF-based composite have been shown to enhance electronic properties, which are useful for amperometric biosensors. In this case, the fibrillary morphology is advantageous for the enzyme loading and ameliorates the capacity for the immobilization of enzymes.112 Metal Nanoparticle-Carbon IL Electrodes (CILEs). One of the most popular applications of transition metals, especially noble metals, is their catalytic activities, which make them suitable materials for the facilitation of various types of chemical/biochemical reactions. The interpolation of metal, such as gold, iridium, platinum, palladium and silver, nanoparticles into carbon and even in metal electrodes has been recently attracting attention.35 The size of the nanoparticles is

Figure 2. Schematic representation of (a) polymerization of a functional IL in the presence of cross-linker and (b) experimental steps for the preparation of PIL-MP containing biomolecule in a W/O emulsion. Reproduced from Nakashima, K.; Kamiya, N.; Koda, D.; Maruyama, T.; Goto, M. Org. Biomol. Chem. 2009, 7, 2353−2358 (ref 43), with permission of The Royal Society of Chemistry.

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ELECTRODE MATERIAL MODIFICATION In addition to the stabilization and activation of biomolecules, ILs can also be used as modifiers or binders to improve the performances of electrode materials. Among the various electrode materials, such as glassy carbon, gold, and carbon paste electrodes (CPEs), modified CPEs have received considerable attention in electrochemical applications.91 A conventional CPE has electrically conducting graphite powder and a nonconductive organic liquid, such as paraffin or Nujol. The displacement of paraffin and Nujol with an IL as a binder and conductor showed attractive, efficient influences on the electrochemical sensor construction and CILE-based biosensors.24,92,93 By replacing a nonconductive organic binder, such as oil, with ILs, low-cost electrodes have been produced. Moreover, the resultant electrodes showed a more uniform conformation than that of traditional CPEs. In traditional oilbased CPEs, the electron transfer can only be accomplished at the carbon−aqueous electrolyte interface, but in the presence of ILs, the electron transfer occurs across the liquid−liquid interface because of the better solubility of polar electrolytes in ILs, which produces a high conductivity and improves the electrochemical performances (Figure 3).15,91 The higher currents (both faradic and capacitive) of CILEs are due to 644

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Analytical Chemistry important to their activity. However, metal nanoparticles suffer from agglomeration. Thermodynamically, large particles are more energetically favored than smaller ones.113,114 Large particles, with a lower surface to volume ratio, present a lower energy state with a lower surface energy.114 Therefore, the system lowers its overall energy by releasing atoms from the surface of the small particles, which diffuse through the solution and attach to the surface of the large particles.114 Consequently, the number of smaller particles decreases as the large particles grow. Thus, stabilizing small metal nanoparticles with additives, which build up a protective layer to shield the particles from each other, is important. 113,114 ILs have a substantial “nanostructure” due to electrostatic, H-bonding, and van der Waals interactions. The structure of ILs, especially imidazolium-based ILs, can induce a three-dimensional, hydrogenbonded network that can entrap nanoparticles, protect them against agglomeration (Figure 4a,b)113−115 and provide a supramolecular IL network that can be used in biosensor structures.116−137

Figure 5. (a) Schematic representation of Au25-mediated glucose oxidation on the surface of IL/Au25/GOx and electron hopping transport through Au25 sites in a composite electrode. (b) Cyclic voltammograms in the presence of glucose between 0 and 1.8 mM. The anodic current responses are proportional to the glucose concentration. Reproduced from Kwak, K.; Kumar, S. S.; Pyo, K.; Lee, D. ACS Nano 2014, 8, 671−679 (ref 138). Copyright 2014 American Chemical Society.

electrochemical biosensors.140 Therefore, it is necessary to modify GR so that the as-prepared multifunctional hybrid materials can have the full benefit of the preferable properties of GR and its functionalized materials.141,142 ILs are effective solubilizing agents for GR nanosheets via π−π interactions,143 and ILs have improved the sensitivity for different types of analytes such as ethanol,144 glucose,145 and ascorbic acid.146 In addition, more recently, IL-functionalized graphene-modified electrodes have been utilized to detect various types of biomolecules.85,147−150

Figure 4. (a) Schematic network structure in 1,3-dialkyl-imidazoliumbased ILs projected in two dimensions. (b) The inclusion of metal nanoparticles (M-NPs) in the supramolecular IL network with electrostatic and steric (= electrosteric) stabilization is indicated through the formation of the suggested primary anion layer forming around the M-NPs. Reproduced from He, Z.; Alexandridis, P. Phys. Chem. Chem. Phys. 2015, 17, 18238−18261 (ref 115), with permission of The Royal Society of Chemistry.

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CONCLUSION ILs are liquid state salts that can be designed and synthesized for special applications by coupling various cations and anions to fine-tune the properties of specific ILs. Most of the electrochemical techniques such as potentiometry, voltammetry, and electrochemical quartz crystal microbalance (EQCM) have been used with success in ILs to produce a new generation of ion-selective sensors, voltammetric devices, and electrochemical biosensors. The promising catalytic potency of ILs and the ability to prepare IL-based composites will greatly boost the development of sensitive, selective, and reproducible electrodes to be used in electrochemical biosensors and other biocompatible devices. The synthesis of ILs with built-in functionalities that can be used as both immobilizing matrixes to entrap proteins and enzymes will provide a good electrocatalytic sensing platform for different substrates. Considering these IL qualities, a fundamental understanding of the underlying biochemistry, surface chemistry, electrochemistry, and technological advances is needed to enhance the

In addition to metal nanoparticle-carbon IL electrodes, previously, an IL of Au25 nanocluster was fabricated and then combined with glucose oxidase (GOx) to obtain an effective electrochemical sensing platform for the glucose analysis.138 The resulted bioelectrode showed an excellent electrochemical performance for the glucose oxidation. Figure 5a,b shows the schematic illustration of IL/Au25/GOx electrode design and electrochemical responses toward glucose.138 Graphene-IL-Based Electrodes. Graphene (GR), a twodimensional form of carbon with a hexagonal lattice structure, is the thinnest material to date among all known materials with a thickness of 0.35 nm.139 GR has many intriguing properties such as excellent conductivity while being a good electronically low-noise material, exceptional biocompatibility, easy functionalization and mass production, and GR and its related composites are promising for potential applications in electrochemical biosensors. However, some intrinsic impediments of GR, such as easy aggregation, poor solubility, and/or processability, are major hindrances to diverse applications for 645

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reliability, portability, and functionality of IL-based biosensors to bring the biosensors to real applications.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone and fax: +90 232 3438624. ORCID

Suna Timur: 0000-0002-3129-8298 Notes

The authors declare no competing financial interest. Biographies Faezeh Ghorbanizamani is a Ph.D. student at the Biochemistry Department at the Faculty of Science of Ege University in Turkey. She received her Master degree in organic chemistry and had been working on the application of ILs in the synthesis and organic reactions. Suna Timur has received her Ph.D. degree of Biochemistry in Ege University in 2001. She is currently a full-time Professor at Department of Biochemistry, Ege University. Her current research focuses on electrochemical sensors and biosensors, nanobiomaterials, nanomedicine, and drug delivery.

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