Next Article in Journal
Natural Variation in the ‘Control Loop’ of BVMOAFL210 and Its Influence on Regioselectivity and Sulfoxidation
Next Article in Special Issue
Green Catalysts: Applied and Synthetic Photosynthesis
Previous Article in Journal
Autocatalytic Fractionation of Wood Hemicelluloses: Modeling of Multistage Operation
Previous Article in Special Issue
Gold-Based Nanoparticles on Amino-Functionalized Mesoporous Silica Supports as Nanozymes for Glucose Oxidation
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Catalysts
Volume 10
Issue 3
10.3390/catal10030338
catalysts-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Recent Advances in Enzyme-Nanostructure Biocatalysts with Enhanced Activity

by
Jing An
1,
Galong Li
1,*,
Yifan Zhang
1,
Tingbin Zhang
2,
Xiaoli Liu
1,
Fei Gao
1,
Mingli Peng
2,
Yuan He
2 and
Haiming Fan
1,2,*
1
School of Chemical Engineering & Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, The College of Life Sciences, Northwest University, Xi’an 710069, China
2
Key Laboratory of Synthetic and Natural Functional Molecule Chemistry of the Ministry of Education, College of Chemistry and Materials Science, Northwest University, Xi’an 710069, China
*
Authors to whom correspondence should be addressed.
Catalysts 2020, 10(3), 338; https://doi.org/10.3390/catal10030338
Submission received: 4 March 2020 / Revised: 14 March 2020 / Accepted: 15 March 2020 / Published: 18 March 2020
(This article belongs to the Special Issue State of the Art and Future Trends in Nanostructured Biocatalysis)
Browse Figures
Review Reports Versions Notes

Abstract

:
Owing to their unique physicochemical properties and comparable size to biomacromolecules, functional nanostructures have served as powerful supports to construct enzyme-nanostructure biocatalysts (nanobiocatalysts). Of particular importance, recent years have witnessed the development of novel nanobiocatalysts with remarkably increased enzyme activities. This review provides a comprehensive description of recent advances in the field of nanobiocatalysts, with systematic elaboration of the underlying mechanisms of activity enhancement, including metal ion activation, electron transfer, morphology effects, mass transfer limitations, and conformation changes. The nanobiocatalysts highlighted here are expected to provide an insight into enzyme–nanostructure interaction, and provide a guideline for future design of high-efficiency nanobiocatalysts in both fundamental research and practical applications.

1. Introduction

The pursuing of efficient supports to improve enzyme performance has been one of the most important directions in biotechnology since the first example of enzyme immobilization in 1916 [1,2,3]. The rapid growth in nanotechnology offers a wealth of opportunities for the successful combination of enzymes with various nanostructured materials, namely enzyme–nanostructure biocatalysts (nanobiocatalysts) [4,5,6,7,8,9]. In contrast to conventional bulk supports, nanostructured supports possess plenty of advantages, such as large specific surface area, reduced mass transfer limitation, ease of surface modifications, unique geometry and size/shape-dependent characteristics. Given these aforementioned advantages, nanobiocatalysts have shown improved stability and recyclability as well as reusability compared to free enzyme. Although immobilization is usually associated with the distortions in the enzyme structure and a decrease in enzyme activity due to the support effect and immobilization methods, nanobiocatalysts have shown a broad spectrum of applications in environmental remediation, biosensing, biomedicine, and industrial biocatalysis [8,10,11].
To attain the high catalytic activity required for nanobiocatalysts in many applications, considerable efforts have been devoted to implementing favorable interactions between enzymes and the nanostructured supports [3,10,11,12,13]. Nanobiocatalysts with increased enzyme activity can be obtained via either covalent binding, adsorption, entrapment, or encapsulation [5,6,14,15]. The structure of nanoscale supports, such as nanoparticles, nanowires, microspheres, metal-organic frameworks, and nanoflowers, has also drawn extensive attention in recent years [5,16,17,18,19,20,21,22]. A great deal of effort has also been made to design nanostructured supports with a variety of components including noble metal (e.g., Au) [23,24], metal oxides (e.g., Cu2O, Fe3O4, SiO2, Ti8O15, alumina) [16,25,26,27,28,29,30,31,32,33], polymer (e.g., Cu2+/PAA/PPEGA matrix, aldehyde-derived Pluronic polymer, polycaprolactone) [34,35,36], metal-organic frameworks (e.g., zeolitic imidazolate framework) [37,38,39], carbon based (e.g., carbon dots, carbon nanotubes) [40,41,42,43,44], and complex compounds (e.g., Cu3(PO4)2∙3H2O, Ca3(PO4)2, Co3(PO4)2·8H2O, Mn3(PO4)2, Ca8H2(PO4)6, Cu4(OH)6)SO4, CaHPO4, Zn3(PO4)2, Mg-Al layered double hydroxide, CdSe/ZnS quantum dots) [17,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59]. These representative supports, which possess unique chemical and physical properties, such as controllable release of ion activator and synergic catalysts and response to external stimuli, are able to regulate the enzyme-support interaction and eventually lead to an unprecedented enhancement in immobilized enzyme activity [7,60,61].
Overall, recent years have witnessed great success in the interactions between artificial nanostructured supports and natural enzymes for enhanced activity. This review will focus on recent advances in this field in the past 10 years, with an emphasis on various mechanisms behind the boosted catalytic activities, including reduced mass transfer limitation, interfacial ion activation, local heating effect, synergistic effects, conformational changes, substrate channeling and so on. A better understanding of the relationship between the characteristics of the nanostructured supports and the enhanced activities of nanobiocatalysts, may provide new insights in designing efficient nanobiocatalysts for various applications.

2. Mechanisms behind Enhanced Activities of Nanobiocatalysts

An overview of recently reported nanobiocatalysts with increased activities is listed in Table 1. Among these, the activity enhancement mechanism is attributed to a favorable interaction between the enzyme and the nanostructured support, which can be roughly categorized into the following strategies: metal ion activation, morphological effects, temperature effects, enhanced electron transfer, conformational modulation, and multi-enzyme cascade reaction (Figure 1). Representative work on each aspect will be discussed here.

2.1. Morphology Effect of Nanoscale Support

The morphology of nanoscale supports has a great impact on the enhancement of enzyme activities and the stability of nanobiocatalysts (Figure 2) [12]. Continuous efforts have yielded many nanostructured supports with various morphologies to provide a large surface area for increased enzyme loading and reduced diffusion resistance [21,79]. Many enzyme immobilization strategies have been developed in consideration of the optimal morphology of supports for minimizing the effect of conformation distortions and the deactivation of immobilized enzymes. As shown in Figure 2, nanobiocatalysts with increased activity are constructed through insertion of nanoparticles into enzyme molecules [23], immobilization of enzymes on the surface of nanoparticle/nanorod/2-dimensional nanomaterials [27,28,34], encapsulation of enzymes in porous supports [37,39], embedding/enveloping enzymes on/in 3-dimensional nanostructured supports [16,48,80]. Horseradish peroxidase was immobilized on a nanoscale DNA scaffold with three addressable sites [72]. The enhanced enzyme activity (>300%) of this nanobiocatalyst was ascribed to preferential binding of the substrates to the minor groove of the double DNA helix. Cytochrome c was encapsulated into spindle-like copper hydroxysulfate nanocrystals, which exhibited a 143-fold increase in catalytic efficiencies (kcat/Km) [55]. The spindle-like nanostructured support with rough surface provided large specific surface area, resulting in an apparent decrease in Km. Therefore, more substances can be accumulated around and within the nanostructured supports for efficient catalytic reactions. Jiang et al. immobilized glucose oxidase on a porous anodic alumina nanochannel membrane [33]. In this case, the O2 molecules can easily go through the nanochannels and participate in the catalytic reaction in an aqueous solution, giving rise to a significant increase in catalytic efficiency (by 80-fold). The construction of a gas-nanochannel-liquid system was shown to boost gas-involving reactions, which introduces a brand-new idea to enhance the activity of immobilized enzymes using gas substrates. Manganese peroxidase was encapsulated in vault nanoparticles, by which the obtained nanobiocatalysts exhibited an enhanced phenol degradation capability three times larger than that of the unpackaged enzymes [80]. The vault nanoparticles with hollow structures were also reported to contribute to an increased catalytic activity of the encapsulated enzymes towards harsh conditions.
Zeng et al enveloped α-amylase on nanoflowers, nanoplates, and parallel hexahedrons (Figure 3A–C), with their reaction rate constants (k) reported to be 16.5 × 10−3, 8.0 × 10−3, and 1.2 × 10−3 s−1, respectively [17]. It was shown that the α-amylase-nanoflowers possess the highest catalytic activity, likely due to their higher surface-to-volume ratios and dramatically reduced mass transfer limitations, as enzymes rested on the surface of a flower petal have much more possibility to react with the substrate. While this is promising, the presence of dead areas in these nanoflowers may hinder their activity enhancement. For a fair comparison of the catalytic activities of various nanobiocatalysts, Fan et al. proposed the use of “specific nanobiocatalyst activity” [16]. The specific enzyme activity is calculated by A = U/P, where P is mg of enzyme. One unit of enzyme activity (U) is the amount of enzyme required to oxidize 1 μmol substrate per minute (or second). The specific nanobiocatalyst activity is defined as A’ = U/B, where B is mg of both enzyme and support. It was reported that the immobilized enzymes with a high specific enzyme activity will actually have a low specific nanobiocatalyst activity. In this work, laccae–Cu2O nanowire mesocrystal hybrid materials exhibited a 2.2-fold increase in specific nanobiocatalyst activity, the highest among the previously reported examples. The nanowire mesocrystal supports display an open octahedra morphology, which is assembled using well-organized anisotropic nanowires as building blocks (Figure 2H). Compared with the compact nanostructured supports, the nanowire mesocrystal has a much larger surface-to-volume ratio and interpenetrating inner channels, which significantly minimize mass transfer limitation (Figure 3F). The 3D ordered spatial arrangement of laccases (Figure 2H) eliminated the phenomena of overlapped nanostructures and provided abundant accessible active sites to substances. In comparison, the laccase–nanowire mesocrystal system attained the highest specific enzyme activities, about 10 and 8 times higher than that of laccase–nanocube and laccase–nanowire systems, respectively (Figure 3D,F). The nanocubes and nanowires were considered to have a greater likelihood to form temporary and permanent aggregations. After that, the disastrous aggregation may exert serious steric hindrance and lead to a significant diffusion resistance, leading to the different diffusion pathways of the substrates, as illustrated in the insets of Figure 3D,F. However, it is worth noting that these 3-dimensional porous supports actually have some disadvantages in increasing the activity of immobilized enzymes. For instance, the immobilized enzymes inside porous supports cannot interact with external substances. The porous support may generate a pH inside the pore that may differ from the optimal pH in the bulk. The enzymes inside the pore are far from optimal pH, causing a decrease in catalytic activity.

2.2. Metal Ions Activation

Metal ions may bind to enzymes and serve as cofactors. About one third of enzymes are known to be metalloenzymes [81]. The metalloenzyme-based nanobiocatalysts have been the most studied because their activities can be activated by the presence of the corresponding metal ions. In such systems, the nanostructured supports can undergo an inherent dissolution–crystallization dynamic process in solution to release the required metal ions, including copper, cobalt and manganese. Metal ions activation of immobilized enzymes has been summarized in Table 2. Ge and the co-workers prepared a laccase-Cu3(PO4)2∙3H2O hybrid nanoflower through a facile and general coprecipitation method, which exhibits a 6.5-fold increase in enzyme activity (Figure 4A) [48]. In this design, Cu2+ ions form complexes with enzyme molecules during the crystal growth process and play an important role in the activation of laccase. Such an activation effect has also been employed to achieve a 5-fold enhancement in the activity of horseradish peroxidase–Cu3(PO4)2∙3H2O hybrid nanoflowers [62]. Liu et al. covalently bound laccase on a Cu2+ adsorbed [poly(acrylic acid)/poly(poly-(ethylene glycol) acrylate)]. The immobilized laccase exhibited both enhanced activity (4.47-fold) and thermal stability [34]. Apart from the Cu2+ activation effect, the Cu2O nanowire mesocrystal support was found to serve as a Cu+/Cu2+ self-sustainable reservoir, which contributed to the remarkably increased enzyme activity, as shown in Figure 4B [16]. The enhancement in activity was mainly due to two factors: the Cu+ can be incorporated into the active center of laccase and the Cu2+ can enhance intramolecular electron transfer. Additionally, cytochrome c was incorporated into the metal-organic frameworks (ZIF-8), in which Zn2+ was considered an important factor for the 10-fold increase in activity [37]. Taken together, the strategy of metal ion activation can provide a vital method in the designing of metalloenzyme-based nanobiocatalysts with efficient catalytic activities.

2.3. Electron Transfer Effect

Enzymatic redox reactions are closely related to the charge transfer process, especially during oxidoreductase-catalyzed processes [42]. Conductive nanostructured supports have been demonstrated as promising candidates to enhance charge transport of redox enzymes. The representative nanomaterials include Au nanoparticles [23], CdS nanorods [82], carbon dots [41], carbon tubes [42], etc. Especially, Au nanoparticles have recently emerged as one of the most prominent supports due to excellent biocompatibility, high specific surface area, and quantum size effects. Au nanoparticles were inserted into laccase, which showed a 1.91-fold enhancement in catalytic activity. The insertion can lead to a looser protein structure and help enzymes to extract electrons from the substrates (Figure 5A) [23]. Kang et al. bound laccase with the -PO3 groups on the surface of carbon dots, and found the groups can combine with the T1 Cu site of laccase, offering increased electron transfer and substrate affinity [41].

2.4. Temperature Effects

The rate of enzymatic reactions is known to be influenced by the temperature of the reaction solution both for general and thermophilic enzymes. Activity measurement of an immobilized enzyme at temperature above the optimal conditions may bring up a significant enhancement in enzyme activity [2]. Adjusting the temperature for improving enzymatic performances has been elaborately investigated in the past decades. Some nanostructured supports can absorb light/electromagnetic waves and convert them into heat for promoting activities of nanobiocatalysts. The effect of temperature on the enhanced activities of immobilized enzymes has been summarized in Table 2 [27,44]. Zhu et al. reported the first example of a temperature-responsive enzyme-polymer nanobiocatalyst, which showed markedly enhanced catalytic activities in organic media at 40 °C [35]. Controlled activation of non-photosensitive enzymatic reactions using a light-to-thermal strategy was also achieved with the help of photosensitive nanostructured supports such as noble metal nanoparticles and semiconductor nanomaterials [83,84]. Blankschien et al. prepared a thermophilic enzyme–Au nanorod nanobiocatalyst that showed an improvement of enzymatic reaction rate of about 60% upon photothermal activation [24]. Although encouraging achievements have been made in light activation of immobilized enzymes, it is important to protect enzymes from deactivation by excessive temperatures and photogenerated holes, as well as reactive oxygen species, especially for constructing a nanobiocatalyst using semiconductor nanomaterials as supports [85].
In comparison with light, magnetic fields can induce the conversion of electromagnetic energy into thermal energy and produce a significant amount of heat around magnetic nanoparticles. The use of magnetic nanostructured supports can also allow for the convenient recovery of nanobiocatalysts [86]. Several interesting examples have successfully harnessed this heating effect in enzyme activation. For example, Knecht et al. prepared a Fe3O4 nanoparticle–enzyme hydrogel network and demonstrated that the thermophilic enzymes could be activated 2-fold via elevated temperature from magnetic actuation [26]. Notably, Xiong et al. developed a ferrimagnetic vortex-domain nanoring-enzyme hybrid and showed that the reaction rate of immobilized enzymes can be boosted up to 1.8-fold without heating up the solution and in a real-time manner (Figure 5B) [27]. This work, for the first time, provides direct biochemical evidence that the localized heating effect from remote magnetic stimulation can be utilized to specifically modulate enzymatic reactions, and may spark future research in spatiotemporally manipulation of intracellular catalysis in living organisms.
Localized heating of enzyme can be produced by the above-mentioned nanostructured supports when exposed to light or alternating magnetic field. The temperature increase at the nanoparticle surface with a sub-nanometer resolution was found to scale down linearly [87]. High local heating may lead to significant damage in enzyme conformation and activity. Hence, it is necessary to weigh the pros and cons of temperature effects on enzyme activity. It may be useful to adjust the distance between enzyme and support or use thermosensitive coupling molecules for enzyme binding.

2.5. Conformational Changes of Immobilized Enzymes

Favorable conformational changes of enzymes induced by either an allosteric effector or nanostructure supports can contribute to improved catalytic activity of nanobiocatalysts [88,89]. Some metal ions have been used to transform the conformation of enzymes to an active form by binding with certain amino acid residues outside enzyme active sites. The so-called allosteric effect is a striking example and a powerful tool to improve the activities of nanobiocatalysts [53]. For example, Zeng et al. reported CaHPO4-α-amylase nanoflowers which have dramatically (38-fold) increased enzyme activities [17]. In this system, Ca2+ ions serve as effectors to bind at an allosteric site, leading to the activation of the enzyme molecules (Figure 5C). It was also found that Mg2+ may act as an allosteric effector of β-galactosidase and was shown to be able to change the secondary structures of enzymes in β-galactosidase/Mg-Al layered double hydroxides [58]. It is clear that every allosteric enzyme is responsive to certain metal ions; consequently, there is no all-encompassing “one size fits all” solution to increase the activity of nanobiocatalysts. The allosteric effectors, apart from metal ions, can be modified on nanostructured supports, which may be a more general and highly effective way to activate allosteric enzymes. In addition, Li et al successfully immobilized lipase from pseudomonas cepacia on siliceous mesocelluar foams (MCF) with different hydrophobicity [71]. With the increase in the surface hydrophobicity of the MCFs, the catalytic activity of lipase was enhanced up to 25-fold. The lipase activation was attributed to hydrophobic interactions between the alkyl groups of MCF and the surface loops of enzymes to produce favorable conformational changes. In other examples, surface modifications of nanostructured supports have been shown to have significant influences not only on enzyme conformation but also on substrate binding in the nanobiocatalysts [12,64,66,90,91,92].

2.6. Multi-Enzyme System

A multi-enzyme system can be obtained by co-immobilizing two or more enzymes, which realize the micro- and nanoscale compartments and enhance the overall activity of the enzymes. There are many strategies for constructing multienzyme catalysis, such as co-immobilization of enzymes, conjugation of natural enzymes with artificial enzymes (i.e. nanozymes), and enhancing the function of enzymes within cell-free metabolic pathways [59,65,77,93,94,95,96,97]. Encapsulation is a common form to maintain a high local concentration of enzymes and protect them from biological damage through proteases. It was reported that five of six encapsulated enzymes inside a DNA nanocage exhibited increased activity and similar Km in comparison with free enzymes [98]. The negatively charged phosphate groups and highly structured water surface on the DNA surface may play a key role in stabilizing the active enzyme conformation.
The activity enhancement phenomenon of multienzyme systems has attracted increasing interest, especially in designing strategies to achieve favorable substrate channeling in cascade reactions [99,100]. Ge et al. and co-workers reported a spatially co-immobilized GOx–HRP system which exhibited dramatically enhanced overall catalytic performance [65]. In this case, the compartmentalization of the two enzymes endow the multi-step cascade reaction with ordered substrate transport, and the formed intermediate concentration gradients make a great contribution to driving and facilitating the reaction. Vranish et al. synthesized a multi-enzymatic coupled system by binding HRP and GOx on quantum dots and for the first time demonstrated a >2-fold improvement in the kcat of the system (Figure 5D) [59]. The challenge is, however, that not all enzymes will manifest activity enhancement when binding to the same quantum dots. Li et al. reported a bio-inspired nanozyme-based multienzyme system which consisted of Au nanoparticles with two enzyme-like activities and ATP synthase, by mimicking mitochondrial oxidative phosphorylation [97]. In this system, the intrinsic glucose oxidase and peroxidase activities of Au nanoparticles provided favorable proton gradient, driving the oxidative phosphorylation of ATP synthase as efficiently as natural mitochondria. In conclusion, nanozymes have been booming in recent years and providing a novel way for designing highly efficient multienzyme systems [60,101,102].
Multi-enzyme systems should be designed to minimize the diffusion of intermediates among the enzymes and increase their overall activity. It is expected that, to create multi-enzyme systems with synergic functions and spatiotemporal multicompartments [103], considerable attention and effort should be devoted to realizing control over the spatial arrangement, number, and class of the enzymes. Some new nanomaterials, such as metal–organic framework nanomaterials, Janus nanoparticles, mesocrystal nanozymes, and aggregation-induced emission nanoparticles, are considered ideal nanostructured supports to organize enzymes in confined microscale or nanoscale environments. In this way, the product of one enzyme can be channeled to act as substrate for the second enzyme. The obtained multi-enzyme system may enhance the overall activity based on high local substrate concentrations [104].

3. Conclusions

Nanobiocatalysts, as a result of the fusion of nanotechnology and biotechnology, exhibit remarkably increased activities, which is a breakthrough in the field of immobilized enzymes. We reviewed the recent development in design and application of these nanobiocatalysts, and summarized underlying the mechanisms of favorable interactions between the nanostructured supports and enzymes, including metal ion activation, enhanced electron transfer, morphological effects, conformational modulation, temperature effects and multi-enzyme systems. To further promote the applications of nanobiocatalysts, the following urgent challenges need to be addressed: (1) an evolutional nanobiocatalyst that can permit the simple recycle and reuse of enzymes; (2) minimizing the “dead areas” of nanobiocatalysts in catalytic reactions to make the hybrid systems more economically friendly; (3) improving the biocompatibility and stability of nanobiocatalysts for in vivo and in vitro biomedical applications; (4) smart nanobiocatalysts that can respond efficiently to remote stimuli for modulating the activities of nanobiocatalysts on demand. We firmly believed that the rapid development of nanotechnology will offer great opportunities to construct novel nanobiocatalysts with real-time-adjustable activity, with widespread applications in biology, medicine and environmental engineering.

Author Contributions

J.A. and G.L. wrote the manuscript and prepared the revised manuscript. Y.Z. and T.Z. discussed the ideas. X.L. and F.G. researched the literature and collected the literature reports. M.P. and Y.H. aided in writing the manuscript. H.F. coordinated the writing and outlined the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. The APC was funded by Northwest University.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 81771981, 81571809, and 31400663) and the Shaanxi Provincial Key Research and Development Program (2019KW-078).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Nelson, J.M.; Griffin, E.G. Adsorption of invertase. J. Am. Chem. Soc. 1916, 38, 1109–1115. [Google Scholar] [CrossRef] [Green Version]
  2. Rodrigues, R.C.; Ortiz, C.; Berenguer-Murcia, Á.; Torres, R.; Fernández-Lafuente, R. Modifying enzyme activity and selectivity by immobilization. Chem. Soc. Rev. 2013, 42, 6290–6307. [Google Scholar] [CrossRef] [PubMed]
  3. Zhang, Y.; Ge, J.; Liu, Z. Enhanced activity of immobilized or chemically modified enzymes. ACS Catal. 2015, 5, 4503–4513. [Google Scholar] [CrossRef]
  4. Vranish, J.N.; Ancona, M.G.; Walper, S.A.; Medintz, I.L. Pursuing the promise of enzymatic enhancement with nanoparticle assemblies. Langmuir 2017, 34, 2901–2925. [Google Scholar] [CrossRef]
  5. Zdarta, J.; Meyer, A.S.; Jesionowski, T.; Pinelo, M. A general overview of support materials for enzyme immobilization: Characteristics, properties, practical utility. Catalysts 2018, 8, 92. [Google Scholar] [CrossRef] [Green Version]
  6. Ge, J.; Lu, D.; Liu, Z.; Liu, Z. Recent advances in nanostructured biocatalysts. Biochem. Eng. J. 2009, 44, 53–59. [Google Scholar] [CrossRef]
  7. Lin, Y.; Chen, Z.; Liu, X.Y. Using inorganic nanomaterials to endow biocatalytic systems with unique features. Trends Biotechnol. 2016, 34, 303–315. [Google Scholar] [CrossRef]
  8. Kim, J.; Grate, J.W.; Wang, P. Nanobiocatalysis and its potential applications. Trends Biotechnol. 2008, 26, 639–646. [Google Scholar] [CrossRef]
  9. Cipolatti, E.P.; Valério, A.; Henriques, R.O.; Moritz, D.E.; Ninow, J.L.; Freire, D.M.G.; Manoel, E.A.; Lafuente, R.F.; Oliverira, D.D. Nanomaterials for biocatalyst immobilization-state of the art and future trends. RSC Adv. 2016, 6, 104675–104692. [Google Scholar] [CrossRef]
  10. Mukhopadhyay, A.; Patra, H.K. Nanoassisted functional modulation of enzymes: Concept and applications. In Advanced Surface Engineering Materials; Wiley: New York, NY, USA, 2016; pp. 349–383. [Google Scholar]
  11. Misson, M.; Zhang, H.; Jin, B. Nanobiocatalyst advancements and bioprocessing applications. J. R. Soc. Interface 2015, 12, 20140891. [Google Scholar] [CrossRef] [Green Version]
  12. Santos, J.C.S.; Barbosa, O.; Ortiz, C.; Berenguer-Murcia, A.; Rodrigues, R.C.; Fernandez-Lafuente, R.F. Importance of the support properties for immobilization or purification of enzymes. ChemCatChem 2015, 7, 2413–2432. [Google Scholar] [CrossRef] [Green Version]
  13. Garcia-Galan, C.; Berenguer-Murcia, Á.; Fernandez-Lafuente, R.; Rodrigues, R.C. Potential of different enzyme immobilization strategies to improve enzyme performance. Adv. Synth. Catal. 2011, 353, 2885–2904. [Google Scholar] [CrossRef]
  14. Sheldon, R.A.; Pelt, S.V. Enzyme immobilisation in biocatalysis: Why, what and how. Chem. Soc. Rev. 2013, 42, 6223–6235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Fernández-Fernández, M.; Sanromán, M.Á.; Moldes, D. Recent developments and applications of immobilized laccase. Biotechnol. Adv. 2013, 31, 1808–1825. [Google Scholar] [CrossRef] [PubMed]
  16. Li, G.; Ma, P.; He, Y.; Zhang, Y.; Luo, Y.; Zhang, C.; Fan, H. Enzyme-nanowire mesocrystal hybrid materials with an extremely high biocatalytic activity. Nano Lett. 2018, 18, 5919–5926. [Google Scholar] [CrossRef] [PubMed]
  17. Wang, L.B.; Wang, Y.C.; He, R.; Zhuang, A.; Wang, X.; Zeng, J.; Hou, J.G. A new nanobiocatalytic system based on allosteric effect with dramatically enhanced enzymatic performance. J. Am. Chem. Soc. 2013, 135, 1272–1275. [Google Scholar] [CrossRef]
  18. Lei, Z.; Gao, C.; Chen, L.; He, Y.; Ma, W.; Lin, Z. Recent advances in biomolecule immobilization based on self-assembly: Organic-inorganic hybrid nanoflowers and metal-organic frameworks as novel substrates. J. Mater. Chem. B 2018, 6, 1581–1594. [Google Scholar] [CrossRef]
  19. Wang, R.; Zhang, Y.; Lu, D.; Ge, J.; Liu, Z.; Zare, R.N. Functional protein-organic/inorganic hybrid nanomaterials. WIREs Nanomed. Nanobiotechnol. 2013, 5, 320–328. [Google Scholar] [CrossRef]
  20. Lee, S.W.; Cheon, S.A.; Kim, M.I.; Park, T.J. Organic-inorganic hybrid nanoflowers: Types, characteristics, and future prospects. J. Nanobiotechnol. 2015, 13, 54. [Google Scholar] [CrossRef] [Green Version]
  21. Zhao, Z.; Zhou, M.C.; Liu, R.L. Recent developments in carriers and non-aqueous solvents for enzyme immobilization. Catalysts 2019, 9, 647. [Google Scholar] [CrossRef] [Green Version]
  22. Wu, X.; Hou, M.; Ge, J. Metal-organic frameworks and inorganic nanoflowers: A type of emerging inorganic crystal nanocarrier for enzyme immobilization. Catal. Sci. Technol. 2015, 5, 5077–5085. [Google Scholar] [CrossRef]
  23. Guo, S.; Li, H.; Liu, J.; Yang, Y.; Kong, W.; Qiao, S.; Huang, H.; Liu, Y.; Kang, Z. Visible-light-induced effects of Au nanoparticle on laccase catalytic activity. ACS Appl. Mater. Interfaces 2015, 7, 20937–20944. [Google Scholar] [CrossRef] [PubMed]
  24. Blankschien, M.D.; Pretzer, L.A.; Huschka, R.; Halas, N.J.; Gonzlez, R.; Wong, M.S. Light-triggered biocatalysis using thermophilic enzyme-gold nanoparticle complexes. ACS Nano 2013, 7, 654–663. [Google Scholar] [CrossRef] [PubMed]
  25. Mukhopadhyay, A.; Dasgupta, A.K.; Chakrabarti, K. Thermostability, pH stability and dye degrading activity of a bacterial laccase are enhanced in the presence of Cu2O nanoparticles. Bioresour. Technol. 2013, 127, 25–36. [Google Scholar] [CrossRef] [PubMed]
  26. Knecht, L.D.; Ali, N.; Wei, Y.; Hilt, J.Z.; Daunert, S. Nanoparticle-mediated remote control of enzymatic activity. ACS Nano 2012, 6, 9079–9086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Xiong, R.; Zhang, W.; Zhang, Y.; Zhang, Y.; Chen, Y.; He, Y.; Fan, H. Remote and real time control of an FVIO-enzyme hybrid nanocatalyst using magnetic stimulation. Nanoscale 2019, 11, 18081–18089. [Google Scholar] [CrossRef]
  28. Corgié, S.C.; Kahawong, P.; Duan, X.; Bowser, D.; Edward, J.B.; Walker, L.P.; Giannelis, E.P. Self-assembled complexes of horseradish peroxidase with magnetic nanoparticles showing enhanced peroxidase activity. Adv. Funct. Mater. 2012, 22, 1940–1951. [Google Scholar] [CrossRef]
  29. Hou, C.; Wang, Y.; Ding, Q.; Jiang, L.; Li, M.; Zhu, W.; Pan, D.; Zhu, H.; Liu, M. Facile synthesis of enzyme-embedded magnetic metal-organic frameworks as a reusable mimic multi-enzyme system: Mimetic peroxidase properties and colorimetric sensor. Nanoscale 2015, 7, 18770–18779. [Google Scholar] [CrossRef] [Green Version]
  30. Xia, T.T.; Liu, C.Z.; Hu, J.H.; Guo, C. Improved performance of immobilized laccase on amine-functioned magnetic Fe3O4 nanoparticles modified with polyethylenimine. Chem. Eng. J. 2016, 295, 201–206. [Google Scholar] [CrossRef]
  31. Luckarift, H.R.; Spain, J.C.; Naik, R.R.; Stone, M.O. Enzyme immobilization in a biomimetic silica support. Nat. Biotechnol. 2004, 22, 211. [Google Scholar] [CrossRef]
  32. Wu, X.; Ou, G.; Yang, C.; Ge, J.; Wu, H. Enhanced enzymatic reactions by solar-to-thermal conversion nanoparticles. Chem. Commun. 2017, 53, 5048–5051. [Google Scholar] [CrossRef] [PubMed]
  33. Mi, L.; Yu, J.; He, F.; Jiang, L.; Wu, Y.; Yang, L.; Han, X.; Li, Y.; Liu, A.; Wei, W.; et al. Boosting gas involved reactions at nanochannel reactor with joint gas-solid-liquid interfaces and controlled wettability. J. Am. Chem. Soc. 2017, 139, 10441–10446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Chen, T.; Xu, Y.; Peng, Z.; Li, A.; Liu, J. Simultaneous enhancement of bioactivity and stability of laccase by Cu2+/PAA/PPEGA matrix for efficient biosensing and recyclable decontamination of pyrocatechol. Anal. Chem. 2017, 89, 2065–2072. [Google Scholar] [CrossRef] [PubMed]
  35. Zhu, J.; Zhang, Y.; Lu, D.; Zare, R.N.; Ge, J.; Liu, Z. Temperature-responsive enzyme-polymer nanoconjugates with enhanced catalytic activities in organic media. Chem. Commun. 2013, 49, 6090–6092. [Google Scholar] [CrossRef]
  36. Song, J.; Kahveci, D.; Chen, M.; Guo, Z.; Xie, E.; Xu, X. Enhanced catalytic activity of lipase encapsulated in PCL nanofibers. Langmuir 2012, 28, 6157–6162. [Google Scholar] [CrossRef]
  37. Lyu, F.; Zhang, Y.; Zare, R.N.; Ge, J.; Liu, Z. One-pot synthesis of protein-embedded metal-organic frameworks with enhanced biological activities. Nano Lett. 2014, 14, 5761–5765. [Google Scholar] [CrossRef]
  38. Du, Y.; Gao, J.; Liu, H.; Zhou, L.; M, L.; He, Y.; Huang, Z.; Jiang, Y. Enzyme@silica nanoflower@metal-organic framework hybrids: A novel type of integrated nanobiocatalysts with improved stability. Nano Res. 2018, 11, 4380–4389. [Google Scholar] [CrossRef]
  39. Li, P.; Moon, S.Y.; Guelta, M.A.; Harvey, S.P.; Hupp, J.T.; Farha, O.K. Encapsulation of a nerve agent detoxifying enzyme by a mesoporous zirconium metal-organic framework engenders thermal and long-term stability. J. Am. Chem. Soc. 2016, 138, 8052–8055. [Google Scholar] [CrossRef]
  40. Li, K.; Wang, J.; He, Y.; Abdulrazaq, M.A.; Yan, Y. Carbon nanotube-lipase hybrid nanoflowers with enhanced enzyme activity and enantioselectivity. J. Biotechnol. 2018, 281, 87–98. [Google Scholar] [CrossRef]
  41. Li, H.; Guo, S.; Li, C.; Huang, H.; Liu, Y.; Kang, Z. Tuning laccase catalytic activity with phosphate functionalized carbon dots by visible light. ACS Appl. Mater. Interfaces 2015, 7, 10004–10012. [Google Scholar] [CrossRef]
  42. Wu, F.; Su, L.; Yu, P.; Mao, L. Role of organic solvents in immobilizing fungus laccase on single-walled carbon nanotubes for improved current response in direct bioelectrocatalysis. J. Am. Chem. Soc. 2017, 139, 1565–1574. [Google Scholar] [CrossRef] [PubMed]
  43. Subrizi, F.; Crucianelli, M.; Grossi, V.; Passacantando, M.; Pesci, L.; Saladino, R. Carbon nanotubes as activating tyrosinase supports for the selective synthesis of catechols. ACS Catal. 2014, 4, 810–822. [Google Scholar] [CrossRef]
  44. Song, Y.; Xu, C.; Wei, W.; Ren, J.; Qu, X. Light regulation of peroxidase activity by spiropyran functionalized carbon nanotubes used for label-free colorimetric detection of lysozyme. Chem. Commun. 2011, 47, 9083–9085. [Google Scholar] [CrossRef] [PubMed]
  45. Altinkaynak, C.; Tavlasoglu, S.; Ÿzdemir, N.; Ocsoy, I. A new generation approach in enzyme immobilization: Organic-inorganic hybrid nanoflowers with enhanced catalytic activity and stability. Enzyme Microb. Technol. 2016, 93, 105–112. [Google Scholar] [CrossRef] [PubMed]
  46. Park, W.M.; Champion, J.A. Colloidal assembly of hierarchically structured porous supraparticles from flower-shaped protein-inorganic hybrid nanoparticles. ACS Nano 2016, 10, 8271–8280. [Google Scholar] [CrossRef] [PubMed]
  47. Pratsinis, A.; Kelesidis, G.A.; Zuercher, S.; Krumeich, F.; Bolisetty, S.; Mezzenga, R.; Leroux, J.C.; Sotiriou, G.A. Enzyme-mimetic antioxidant luminescent nanoparticles for highly sensitive hydrogen peroxide biosensing. ACS Nano 2017, 11, 12210–12218. [Google Scholar] [CrossRef]
  48. Ge, J.; Lei, J.; Zare, R.N. Protein-inorganic hybrid nanoflowers. Nat. Nanotechnol. 2012, 7, 428–432. [Google Scholar] [CrossRef]
  49. Batule, B.S.; Park, K.S.; Kim, M.I.; Park, H.G. Ultrafast sonochemical synthesis of protein-inorganic nanoflowers. Int. J. Nanomed. 2015, 10, 137–142. [Google Scholar]
  50. Rong, J.; Zhang, T.; Qiu, F.; Zhu, Y. Preparation of efficient, stable, and reusable laccase-Cu3(PO4)2 hybrid microspheres based on copper foil for decoloration of congo red. ACS Sustain. Chem. Eng. 2017, 5, 4468–4477. [Google Scholar] [CrossRef]
  51. Lang, X.; Zhu, L.; Gao, Y.; Wheeldon, I. Enhancing enzyme activity and immobilization in nanostructured inorganic-enzyme complexes. Langmuir 2017, 33, 9073–9080. [Google Scholar] [CrossRef]
  52. Yin, Y.; Xiao, Y.; Lin, G.; Xiao, Q.; Lin, Z.; Cai, Z. An enzyme-inorganic hybrid nanoflower based immobilized enzyme reactor with enhanced enzymatic activity. J. Mater. Chem. B 2015, 3, 2295–2300. [Google Scholar] [CrossRef]
  53. Han, L.; Liu, A. Novel cell-inorganic hybrid catalytic interfaces with enhanced enzymatic activity and stability for sensitive biosensing of paraoxon. ACS Appl. Mater. Interfaces 2017, 9, 6894–6901. [Google Scholar] [CrossRef] [PubMed]
  54. Duan, L.; Li, H.; Zhang, Y. Synthesis of hybrid nanoflower-based carbonic anhydrase for enhanced biocatalytic activity and stability. ACS Omega 2018, 3, 18234–18241. [Google Scholar] [CrossRef] [Green Version]
  55. Li, Z.; Ding, Y.; Li, S.; Jiang, Y.; Liu, Z.; Ge, J. Highly active, stable and self-antimicrobial enzyme catalysts prepared by biomimetic mineralization of copper hydroxysulfate. Nanoscale 2016, 8, 17440–17445. [Google Scholar] [CrossRef] [PubMed]
  56. Zhang, B.; Li, P.; Zhang, H.; Wang, H.; Li, X.; Tian, L.; Ali, N.; Ali, Z. Preparation of lipase/Zn3(PO4)2 hybrid nanoflower and its catalytic performance as an immobilized enzyme. Chem. Eng. J. 2016, 291, 287–297. [Google Scholar] [CrossRef]
  57. Ye, R.; Zhu, C.; Song, Y.; Song, J.; Fu, S.; Lu, Q.; Yang, X.; Zhu, M.J.; Du, D.; Li, H.; et al. One-pot bioinspired synthesis of all-inclusive protein-protein nanoflowers for point-of-care bioassay: Detection of E. coli O157: H7 from milk. Nanoscale 2016, 8, 18980–18986. [Google Scholar] [CrossRef]
  58. Wang, M.; Huang, S.W.; Xu, D.; Bao, W.J.; Xia, X.H. Ultrahigh enzyme activity assembled in layered double hydroxides via Mg2+-allosteric effector. Anal. Chem. 2015, 87, 5831–5836. [Google Scholar] [CrossRef]
  59. Vranish, J.N.; Ancona, M.G.; Oh, E.; Susumu, K.; Medintz, I.L. Enhancing coupled enzymatic activity by conjugating one enzyme to a nanoparticle. Nanoscale 2017, 9, 5172–5187. [Google Scholar] [CrossRef] [PubMed]
  60. Liang, M.; Yan, X. Nanozymes: From new concepts, mechanisms, and standards to applications. Acc. Chem. Res. 2019, 52, 2190–2200. [Google Scholar] [CrossRef]
  61. Torres-Salas, P.; Monte-Martinez, A.; Cutiño-Avila, B.; Rodriguez-Colinas, B.; Alcalde, M.; Ballesteros, A.O.; Plou, F.J. Immobilized biocatalysts: Novel approaches and tools for binding enzymes to supports. Adv. Mater. 2011, 23, 5275–5282. [Google Scholar] [CrossRef] [Green Version]
  62. Lin, Z.; Xiao, Y.; Yin, Y.; Hu, W.; Liu, W.; Yang, H. Facile synthesis of enzyme-inorganic hybrid nanoflowers and its application as a colorimetric platform for visual detection of hydrogen peroxide and phenol. ACS Appl. Mater. Interfaces 2014, 6, 10775–10782. [Google Scholar] [CrossRef] [PubMed]
  63. Zhu, L.; Gong, L.; Zhang, Y.; Wang, R.; Ge, J.; Liu, Z.; Zare, R.N. Rapid detection of phenol using a membrane containing laccase nanoflowers. Chem. Asian J. 2013, 8, 2358–2360. [Google Scholar] [CrossRef] [PubMed]
  64. Forde, J.; Tully, E.; Vakurov, A.; Gibson, T.D.; Millner, P.; Ó’Fágáin, C. Chemical modification and immobilisation of laccase from Trametes hirsuta and from Myceliophthora thermophila. Enzyme Microb. Technol. 2010, 46, 430–437. [Google Scholar] [CrossRef] [PubMed]
  65. Li, Z.; Zhang, Y.; Su, Y.; Ouyang, P.; Ge, J.; Liu, Z. Spatial co-localization of multi-enzymes by inorganic nanocrystal-protein complexes. Chem. Commun. 2014, 50, 12465–12468. [Google Scholar] [CrossRef]
  66. Cui, J.; Zhao, Y.; Liu, R.; Zhong, C.; Jia, S. Surfactant-activated lipase hybrid nanoflowers with enhanced enzymatic performance. Sci. Rep. 2016, 6, 27928. [Google Scholar] [CrossRef] [Green Version]
  67. Zheng, L.; Sun, Y.; Wang, J.; Huang, H.; Geng, X.; Tong, Y.; Wang, Z. Preparation of a flower-like immobilized D-Psicose 3-epimerase with enhanced catalytic performance. Catalysts 2018, 8, 468. [Google Scholar] [CrossRef] [Green Version]
  68. Torres, O.S.; Vazquez, L.B.; Simakov, A.; Duhalt, R.V. Enhanced laccase activity of biocatalytic hybrid copper hydroxide nanocages. Enzyme Microb. Technol. 2019, 128, 59–66. [Google Scholar] [CrossRef]
  69. Wang, R.; Zhang, Y.; Huang, J.; Lu, D.; Ge, J.; Liu, Z. Substrate imprinted lipase nanogel for one-step synthesis of chloramphenicol palmitate. Green Chem. 2013, 15, 1155–1158. [Google Scholar] [CrossRef]
  70. Zhang, Y.; Dai, Y.; Hou, M.; Li, T.; Ge, J.; Liu, Z. Chemo-enzymatic synthesis of valrubicin using Pluronic conjugated lipase with temperature responsiveness in organic media. RSC Adv. 2013, 3, 22963–22966. [Google Scholar] [CrossRef]
  71. Jin, Q.; Jia, G.; Zhang, Y.; Yang, Q.; Li, C. Hydrophobic surface induced activation of Pseudomonas cepacia lipase immobilized into mesoporous silica. Langmuir 2011, 27, 12016–12024. [Google Scholar] [CrossRef]
  72. Lin, J.L.; Wheeldon, I. Kinetic enhancements in DNA-enzyme nanostructures mimic the sabatier principle. ACS Catal. 2013, 3, 560–564. [Google Scholar] [CrossRef]
  73. Somturk, B.; Yilmaz, I.; Altinkaynak, C.; Karatepe, A.; Özdemir, N.; Ocsoy, I. Synthesis of urease hybrid nanoflowers and their enhanced catalytic properties. Enzyme Microb. Technol. 2016, 86, 134–142. [Google Scholar] [CrossRef] [PubMed]
  74. Patel, S.K.S.; Otari, S.V.; Kang, Y.C.; Lee, J.K. Protein-inorganic hybrid system for efficient his-tagged enzymes immobilization and its application in L-xylulose production. RSC Adv. 2017, 7, 3488–3494. [Google Scholar] [CrossRef] [Green Version]
  75. Zhang, S.; Wu, Z.; Chen, G.; Wang, Z. An improved method to encapsulate laccase from Trametes versicolor with enhanced stability and catalytic activity. Catalysts 2018, 8, 286. [Google Scholar] [CrossRef] [Green Version]
  76. Fang, X.; Zhang, C.; Qian, X.; Yu, D. Self-assembled 2,4-dichlorophenol hydroxylase-inorganic hybrid nanoflowers with enhanced activity and stability. RSC Adv. 2018, 8, 20976–20981. [Google Scholar] [CrossRef] [Green Version]
  77. 77Vranish, J.N.; Ancona, M.G.; Oh, E.; Susumu, K.; Aragonés, G.L.; Breger, J.C.; Walper, S.A.; Medintz, I.L. Enhancing coupled enzymatic activity by colocalization on nanoparticle surfaces: Kinetic evidence for directed channeling of intermediates. ACS Nano 2018, 12, 7911–7926. [Google Scholar] [CrossRef]
  78. Ibrahim, A.S.S.; Al-Salamah, A.A.; El-Toni, A.M.; Almaary, K.S.; El-Tayeb, M.A.; Elbadawi, Y.B.; Antranikian, G. Enhancement of alkaline protease activity and stability via covalent immobilization onto hollow core-mesoporous shell silica nanospheres. Int. J. Mol. Sci. 2016, 17, 184. [Google Scholar] [CrossRef] [Green Version]
  79. Zhou, Z.; Taylor, R.N.K.; Kullmann, S.; Bao, H. Mesoporous organosilicas with large cage-like pores for high efficiency immobilization of enzymes. Adv. Mater. 2011, 23, 2627–2632. [Google Scholar] [CrossRef]
  80. Wang, M.; Abad, D.; Kickhoefer, V.A.; Rome, L.H.; Mahendra, S. Vault nanoparticles packaged with enzymes as an efficient pollutant biodegradation technology. ACS Nano 2015, 9, 10931–10940. [Google Scholar] [CrossRef]
  81. Schwizer, F.; Okamoto, Y.; Heinisch, T.; Gu, Y.; Pellizzoni, M.M.; Lebrun, V.; Reuter, R.; Köhler, V.; Lewis, J.C.; Ward, T.R. Artificial metalloenzymes: Reaction scope and optimization strategies. Chem. Rev. 2018, 118, 142–231. [Google Scholar] [CrossRef] [Green Version]
  82. Brown, K.A.; Wilker, M.B.; Boehm, M.; Dukovic, G.; King, P.W. Characterization of photochemical processes for H2 production by CdS nanorod-[FeFe] hydrogenase complexes. J. Am. Chem. Soc. 2012, 134, 5627–5636. [Google Scholar] [CrossRef] [PubMed]
  83. Kohse, S.; Neubauer, A.; Razidis, A.; Lochbrunner, S.; Krag, U. Photoswitching of enzyme activity by laser-induced pH-jump. J. Am. Chem. Soc. 2013, 135, 9407–9411. [Google Scholar] [CrossRef] [PubMed]
  84. Wang, C.; Zhang, Q.; Wang, X.; Chang, H.; Zhang, S.; Tang, Y.; Xu, J.; Qi, R.; Cheng, Y. Dynamic modulation of enzyme activity by near-infrared light. Angew. Chem. Int. Ed. 2017, 56, 6767–6772. [Google Scholar] [CrossRef]
  85. Zhang, S.; Shi, J.; Sun, Y.; Wu, Y.; Zhang, Y.; Cai, Z.; Chen, Y.; You, C.; Han, P.; Jiang, Z. Artificial thylakoid for the coordinated photoenzymatic reduction of carbon dioxide. ACS Catal. 2019, 9, 3913–3925. [Google Scholar] [CrossRef]
  86. Alarcón-Correa, M.; Günther, J.P.; Troll, J.; Kadiri, V.M.; Bill, J.; Fischer, P.; Rothenstein, D. Self-assembled phage-based colloids for high localized enzymatic activity. ACS Nano 2019, 13, 5810–5815. [Google Scholar] [CrossRef] [PubMed]
  87. Riedinger, A.; Cuardia, P.; Curcio, A.; Garcia, M.A.; Cingolani, R.; Manna, L.; Rellegrino, T. Subnanometer local temperature probing and remotely controlled drug release based on azo-functionalized iron oxide nanoparticles. Nano Lett. 2013, 13, 2399–2406. [Google Scholar] [CrossRef]
  88. Secundo, F. Conformational changes of enzymes upon immobilisation. Chem. Soc. Rev. 2013, 42, 6250–6261. [Google Scholar] [CrossRef]
  89. Darby, J.F.; Atobe, M.; Firth, J.D.; Bond, P.; Davies, G.J.; O’Brien, P.; Hubbard, R.E. Increase of enzyme activity through specific covalent modification with fragments. Chem. Sci. 2017, 8, 7772–7779. [Google Scholar] [CrossRef] [Green Version]
  90. Liu, B.; Liu, J. Surface modification of nanozymes. Nano Res. 2017, 10, 1125–1148. [Google Scholar] [CrossRef]
  91. Sheldon, R.A.; Pereira, P.C. Biocatalysis engineering: The big picture. Chem. Soc. Rev. 2017, 46, 2678–2691. [Google Scholar] [CrossRef]
  92. Rueda, N.; Santos, J.C.S.; Ortiz, C.; Torres, R.; Barbosa, O.; Rodrigues, R.C.; Berenguer-Murcia, Á.; Fernandez-Lafuente, R. Chemical modification in the design of immobilized enzyme biocatalysts: Drawbacks and opportunities. Chem. Rec. 2016, 16, 1436–1455. [Google Scholar] [CrossRef] [PubMed]
  93. Görbe, T.; Gustafson, K.P.J.; Verho, O.; Kervefors, G.; Zheng, H.; Zou, X.; Johnston, E.V.; Bäckvall, J.E. Design of a Pd(0)-CalB CLEA biohybrid catalyst and its application in a one-pot cascade reaction. ACS Catal. 2017, 7, 1601–1605. [Google Scholar] [CrossRef] [Green Version]
  94. Zhu, X.; Huang, J.; Liu, J.; Zhang, H.; Jiang, J.; Yu, R. A dual enzyme-inorganic hybrid nanoflower incorporated microfluidic paper-based analytic device (μPAD) biosensor for sensitive visualized detection of glucose. Nanoscale 2017, 9, 5658–5663. [Google Scholar] [CrossRef] [PubMed]
  95. Liang, H.; Jiang, S.; Yuan, Q.; Li, G.; Wang, F.; Zhang, Z.; Liu, J. Co-immobilization of multiple enzymes by metal coordinated nucleotide hydrogel nanofibers: Improved stability and an enzyme cascade for glucose detection. Nanoscale 2016, 8, 6071–6078. [Google Scholar] [CrossRef] [PubMed]
  96. Sun, J.; Ge, J.; Liu, W.; Lan, M.; Zhang, H.; Wang, P.; Wang, Y.; Niu, Z. Multi-enzyme co-embedded organic-inorganic hybrid nanoflowers: Synthesis and application as a colorimetric sensor. Nanoscale 2014, 6, 255–262. [Google Scholar] [CrossRef] [PubMed]
  97. Xu, Y.; Fei, J.; Li, G.; Yuan, T.; Xu, X.; Li, J. Nanozyme-catalyzed cascade reactions for mitochondria-mimicking oxidative phosphorylation. Angew. Chem. Int. Edit. 2019, 58, 5572–5576. [Google Scholar] [CrossRef]
  98. Zhao, Z.; Fu, J.; Dhakal, S.; Johnson-Buk, A.; Liu, M.; Zhang, T.; Woodbury, N.W.; Liu, Y.; Walter, N.G.; Yan, H. Nanocaged enzymes with enhanced catalytic activity and increased stability against protease digestion. Nat. Commun. 2016, 7, 10619. [Google Scholar] [CrossRef] [Green Version]
  99. Sulman, E.M.; Matveeva, V.G.; Bronstein, L.M. Design of biocatalysts for efficient catalytic processes. Curr. Opin. Chem. Eng. 2019, 26, 1–8. [Google Scholar] [CrossRef]
  100. Hwang, E.T.; Lee, S. Multienzymatic cascade reactions via enzyme complex by immobilization. ACS Catal. 2019, 9, 4402–4425. [Google Scholar] [CrossRef]
  101. Wei, H.; Wang, E. Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes. Chem. Soc. Rev. 2013, 42, 6060–6093. [Google Scholar] [CrossRef]
  102. Wu, J.; Wang, X.; Wang, Q.; Lou, Z.; Li, S.; Zhu, Y.; Wei, H. Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes (II). Chem. Soc. Rev. 2019, 48, 1004–1076. [Google Scholar] [CrossRef] [PubMed]
  103. Wang, H.; Zhao, Z.; Liu, Y.; Shao, C.; Bian, F.; Zhao, Y. Biomimetic enzyme cascade reaction system in microfluidic electrospray microcapsules. Sci. Adv. 2018, 4, eaat2816. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  104. Chen, W.; Vázquez-González, M.; Zoabi, A.; Abu-Reziq, R.; Willner, I. Biocatalytic cascades driven by enzymes encapsulated in metal-organic framework nanoparticles. Nat. Catal. 2018, 1, 689–695. [Google Scholar] [CrossRef]
Catalysts 10 00338 g001 550
Figure 1. Design of nanobiocatalysts with favorable interactions between enzymes and nanostructured supports for enhanced activities.
Figure 1. Design of nanobiocatalysts with favorable interactions between enzymes and nanostructured supports for enhanced activities.
Catalysts 10 00338 g001
Catalysts 10 00338 g002 550
Figure 2. Representative morphologies of nanobiocatalysts with increased activities. (A) Insertion of nanoparticles into enzyme molecules. (B–D) Immobilization of enzymes on the surface of nanoparticle/nanorod/2 dimensional nanomaterial. (E) Encapsulation of enzymes in porous supports. (F–H) Embedding/enveloping enzymes on/in 3-dimensional nanostructured supports.
Figure 2. Representative morphologies of nanobiocatalysts with increased activities. (A) Insertion of nanoparticles into enzyme molecules. (B–D) Immobilization of enzymes on the surface of nanoparticle/nanorod/2 dimensional nanomaterial. (E) Encapsulation of enzymes in porous supports. (F–H) Embedding/enveloping enzymes on/in 3-dimensional nanostructured supports.
Catalysts 10 00338 g002
Catalysts 10 00338 g003 550
Figure 3. SEM images of CaHPO4-α-amylase nanobiocatalysts, (A) nanoflowers, (B) nanoplates, and (C) parallel hexahedrons. Reconstructed with permission from Ref. [17], Copyright (2013) American Chemical Society. SEM images of Cu2O–laccase nanobiocatalysts, (D) nanocubes, (E) nanowires, and (F) nanowire mesocrytal, insets are the schematic illustrations of the plausible substrate diffusion pathways for these hybrid materials. Reconstructed with permission from Ref. [16], copyright (2018) American Chemical Society.
Figure 3. SEM images of CaHPO4-α-amylase nanobiocatalysts, (A) nanoflowers, (B) nanoplates, and (C) parallel hexahedrons. Reconstructed with permission from Ref. [17], Copyright (2013) American Chemical Society. SEM images of Cu2O–laccase nanobiocatalysts, (D) nanocubes, (E) nanowires, and (F) nanowire mesocrytal, insets are the schematic illustrations of the plausible substrate diffusion pathways for these hybrid materials. Reconstructed with permission from Ref. [16], copyright (2018) American Chemical Society.
Catalysts 10 00338 g003
Catalysts 10 00338 g004 550
Figure 4. (A) Formation process of enzyme-incorporating Cu3(PO4)2·3H2O nanoflowers, comprising three steps: nucleation and formation of primary crystals, growth of crystals, formation of nanoflowers. Reprinted with permission from Ref. [48]. Copyright (2012) Nature Publishing Group. (B) Bioinspired fabrication of enzyme–nanowire mesocrystal hybrid materials by mimicking natural rough endoplasmic reticulum. Reconstructed with permission from Ref. [16], copyright (2018) American Chemical Society.
Figure 4. (A) Formation process of enzyme-incorporating Cu3(PO4)2·3H2O nanoflowers, comprising three steps: nucleation and formation of primary crystals, growth of crystals, formation of nanoflowers. Reprinted with permission from Ref. [48]. Copyright (2012) Nature Publishing Group. (B) Bioinspired fabrication of enzyme–nanowire mesocrystal hybrid materials by mimicking natural rough endoplasmic reticulum. Reconstructed with permission from Ref. [16], copyright (2018) American Chemical Society.
Catalysts 10 00338 g004
Catalysts 10 00338 g005 550
Figure 5. (A) Schematic of the Au–laccase hybrids with enhanced electron transfer. Reconstructed with permission from Ref. [23], Copyright (2015) American Chemical Society. (B) Illustration of the FVIO-β-Gal hybrids and the experimental set-up, the activities were tuned by AFM-triggered local heating. Reprinted with permission from Ref. [27]. Copyright (2019) RSC Pub. (C) The α-amylase-CaHPO4 nanoflower nanobiocatalyst Ca2+ binds to allosteric sites in inactive α-amylase and generates active α-amylase. Reproduced with permission from Ref. [17], copyright 2013, American Chemical Society. (D) Diagram of the GOX/HRP–CdSe/ZnS QDs system with enhanced coupled enzymatic activity. Reconstructed with permission from Ref. [59], copyright (2017) RSC Pub.
Figure 5. (A) Schematic of the Au–laccase hybrids with enhanced electron transfer. Reconstructed with permission from Ref. [23], Copyright (2015) American Chemical Society. (B) Illustration of the FVIO-β-Gal hybrids and the experimental set-up, the activities were tuned by AFM-triggered local heating. Reprinted with permission from Ref. [27]. Copyright (2019) RSC Pub. (C) The α-amylase-CaHPO4 nanoflower nanobiocatalyst Ca2+ binds to allosteric sites in inactive α-amylase and generates active α-amylase. Reproduced with permission from Ref. [17], copyright 2013, American Chemical Society. (D) Diagram of the GOX/HRP–CdSe/ZnS QDs system with enhanced coupled enzymatic activity. Reconstructed with permission from Ref. [59], copyright (2017) RSC Pub.
Catalysts 10 00338 g005
Table
Table 1. Recent nanobiocatalysts with increased activities, constructed by various nanostructure supports and enzymes.
Table 1. Recent nanobiocatalysts with increased activities, constructed by various nanostructure supports and enzymes.
EnzymesSupportsIncreased Activities
(Folds)		Ref.
LaccaseCu3(PO4)2 nanoflower6.50[48]
Horseradish peroxidiseCu3(PO4)2 nanoflower5.06[62]
LaccaseCu3(PO4)2 nanoflower1.50[49]
LipasePolycaprolactone nanofiber14.00[36]
LaccaseAu nanoparticle1.91[23]
LaccaseCarbon dots1.92[41]
LaccaseCu2+/PAA/PPEGA4.47[34]
LaccaseSingle-walled carbon nanotube6.00[42]
LaccaseCu3(PO4)2 hybrid microsphere3.60[50]
LaccaseMembrane/nanoflower2.00[63]
LaccaseMesoporous silica nanoparticle1.20[64]
LaccaseCu2O nanoparticle4.00[25]
α-amylaseCaHPO4 nanoflower37.5[17]
β-galactosidaseMg-Al layered double hydroxide30.00[58]
α-chymotrypsinCa3(PO4)2 nanoflower2.66[52]
Horseradish peroxidase,
Glucose oxidase		Cu3(PO4)2·3H2O nanocrystal1.40
3.10		[65]
Cytochrome cZIF-8 metal-organic framework10.00[37]
Lipase,
Cytochrome c		Pluronic polymer67.00,
670.0		[35]
L-2-HADST dehalogenaseFe3O4 nanoparticles/hydrogel2.00[26]
LipaseCu3(PO4)2 nanoflower4.60[66]
Organophosphorus hydrolaseCo3(PO4)2·8H2O nanocrystal3.00[53]
Amylase,
Cellulase,
Lipase		Ti8O15 nanoparticle13.00,
5.00,
12.00		[32]
Glucose oxidaseCdSe/ZnS quantum dot2.00[59]
Carbonic anhydraseCu3(PO4)2 nanoflower,
Ca8H2(PO4)6 nanoflower		2.86,
1.49		[54]
D-psicose 3-epimeraseCo3(PO4)2 nanoflower7.20[67]
LipaseCarbon nanotube,
Cu3(PO4)2 nanoflower		68.00,
51.00		[40]
LaccaseCu2O nanowire mesocystal10.00[16]
LaccaseCu(OH)2 nanocage18.00[68]
β-galactosidaseFe3O4 nanoring1.80[27]
LipasePolyacrylamide nanogel2.00[69]
LipasePluronic polymer11.00[70]
Lipasesiliceous mesocellular foam25.00[71]
Horseradish peroxidaseDNA scaffold>3.00[72]
Horseradish peroxidaseMagnetic nanoparticle10.00[28]
Cytochrome cCopper hydroxysulfate143.00[55]
LaccaseFe3O4-NH2-PEI
Fe3O4-NH2		101.33
74.45		[30]
Glucose oxidaseAnodic alumina nanochannel80.00[33]
LipaseZn3(PO4)2 hybrid nanoflower1.47[56]
InvertaseCaHPO4 hybrid nanoflower2.03[57]
UreaseCu3(PO4)2·3H2O nanoflower40.00[73]
L-arabinitol 4-dehydrogenase,
NADH oxidase		Cu3(PO4)2·3H2O nanoflower2.46,
1.44		[74]
LaccaseCopper alginate3.00[75]
HydroxylaseCu3(PO4)2·3H2O nanoflower1.62[76]
Pyruvate kinase/lactate dehydrogenaseSemiconductor quantum dot>50.00[77]
Alkaline proteaseHollow silica nanosphere2.40[78]
Table
Table 2. The effects of metal ion and temperature on the enhanced activities of immobilized enzymes.
Table 2. The effects of metal ion and temperature on the enhanced activities of immobilized enzymes.
EnzymesEffectsIncreased Activities
(Folds)		Ref.
Laccase,
carbonic anhydrase		Cu2+6.50
2.60		[48]
LaccaseCu2+4.47[34]
LaccaseCu2+3.60[50]
LaccaseCu2+4.00[25]
α-amylaseCa2+ (Allosteric Effect)37.5[17]
β-galactosidaseMg2+ (Allosteric Effect)30.00[58]
Cytochrome cZn2+10.00[37]
Organophosphorus hydrolaseCo2+ (Allosteric Effect)3.00[53]
Carbonic anhydraseCu2+,
Ca2+		2.86,
1.49		[54]
UreaseCu2+40.00[73]
D-psicose 3-epimeraseCo2+7.20[67]
LaccaseCu+ and Cu2+10.00[16]
LaccaseCu2+18.00[68]
Lipase,
Cytochrome c		Temperature responsiveness
in organic solvents		67.00,
670.0		[35]
L-2-HADST dehalogenaseMagnetothermal effect2.00[26]
LaccaseIncreased temperature by local surface plasma resonance effect1.91[23]
Amylase,
Cellulase,
Lipase		Solar-to-thermal conversion13.00,
5.00,
12.00		[32]
β-galactosidaseMagnetothermal effect1.80[27]
LipaseTemperature responsiveness
in organic media		11.00[70]

Share and Cite

MDPI and ACS Style

An, J.; Li, G.; Zhang, Y.; Zhang, T.; Liu, X.; Gao, F.; Peng, M.; He, Y.; Fan, H. Recent Advances in Enzyme-Nanostructure Biocatalysts with Enhanced Activity. Catalysts 2020, 10, 338. https://doi.org/10.3390/catal10030338

AMA Style

An J, Li G, Zhang Y, Zhang T, Liu X, Gao F, Peng M, He Y, Fan H. Recent Advances in Enzyme-Nanostructure Biocatalysts with Enhanced Activity. Catalysts. 2020; 10(3):338. https://doi.org/10.3390/catal10030338

Chicago/Turabian Style

An, Jing, Galong Li, Yifan Zhang, Tingbin Zhang, Xiaoli Liu, Fei Gao, Mingli Peng, Yuan He, and Haiming Fan. 2020. "Recent Advances in Enzyme-Nanostructure Biocatalysts with Enhanced Activity" Catalysts 10, no. 3: 338. https://doi.org/10.3390/catal10030338

APA Style

An, J., Li, G., Zhang, Y., Zhang, T., Liu, X., Gao, F., Peng, M., He, Y., & Fan, H. (2020). Recent Advances in Enzyme-Nanostructure Biocatalysts with Enhanced Activity. Catalysts, 10(3), 338. https://doi.org/10.3390/catal10030338

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop