Microenvironmental engineering: An effective strategy for tailoring enzymatic activities

doi:10.1016/j.cjche.2020.04.010

摘要/Abstract

摘要： Rationally, engineering a favorable physicochemical microenvironment for enzymes has recently emerged as an effective strategy to improve their catalytic performance. In this review, we discuss four microenvironmental effects according to the mechanism of action: localizing and excluding reactants and regulators, regulating microenvironmental pH, creating a water-like microenvironment, and increasing the local temperature. These mechanisms are enzyme-independent and can in principle be used in combination to tailor enzyme behaviors, offering new approaches to enabling, enhancing, and regulating enzyme catalysis in diverse applications without the need for genetic engineering.

关键词: Biocatalysis, Enzyme, Microenvironment, Activity enhancement

Abstract: Rationally, engineering a favorable physicochemical microenvironment for enzymes has recently emerged as an effective strategy to improve their catalytic performance. In this review, we discuss four microenvironmental effects according to the mechanism of action: localizing and excluding reactants and regulators, regulating microenvironmental pH, creating a water-like microenvironment, and increasing the local temperature. These mechanisms are enzyme-independent and can in principle be used in combination to tailor enzyme behaviors, offering new approaches to enabling, enhancing, and regulating enzyme catalysis in diverse applications without the need for genetic engineering.

Key words: Biocatalysis, Enzyme, Microenvironment, Activity enhancement

Yifei Zhang, Henry Hess. Microenvironmental engineering: An effective strategy for tailoring enzymatic activities[J]. 中国化学工程学报, 2020, 28(8): 2028-2036.

Yifei Zhang, Henry Hess. Microenvironmental engineering: An effective strategy for tailoring enzymatic activities[J]. Chinese Journal of Chemical Engineering, 2020, 28(8): 2028-2036.

参考文献

[1] M.A. Huffman, A. Fryszkowska, O. Alvizo, M. Borra-Garske, K.R. Campos, K.A. Canada, P.N. Devine, D. Duan, J.H. Forstater, S.T. Grosser, H.M. Halsey, G.J. Hughes, J. Jo, L.A. Joyce, J.N. Kolev, J. Liang, K.M. Maloney, B.F. Mann, N.M. Marshall, M. McLaughlin, J.C. Moore, G.S. Murphy, C.C. Nawrat, J. Nazor, S. Novick, N.R. Patel, A. Rodriguez-Granillo, S.A. Robaire, E.C. Sherer, M.D. Truppo, A.M. Whittaker, D. Verma, L. Xiao, Y. Xu, H. Yang, Design of an in vitro biocatalytic cascade for the manufacture of islatravir, Science 366(2019) 1255-1259.
[2] R.A. Sheldon, Engineering a more sustainable world through catalysis and green chemistry, J. R. Soc. Interface 13(2016) 20160140.
[3] A. Bruggink, E.C. Roos, E. de Vroom, Penicillin acylase in the industrial production of beta-lactam antibiotics, Org. Proc. Res. Dev. 2(1998) 128-133.
[4] R. DiCosimo, J. McAuliffe, A.J. Poulose, G. Bohlmann, Industrial use of immobilized enzymes, Chem. Soc. Rev. 42(2013) 6437-6474.
[5] S. Zhao, R. Kumar, A. Sakai, M.W. Vetting, B.M. Wood, S. Brown, J.B. Bonanno, B.S. Hillerich, R.D. Seidel, P.C. Babbitt, S.C. Almo, J.V. Sweedler, J.A. Gerlt, J.E. Cronan, M.P. Jacobson, Discovery of new enzymes and metabolic pathways by using structure and genome context, Nature 502(2013) 698-702.
[6] F.H. Arnold, Directed evolution:Bringing new chemistry to life, Angew. Chem. Int. Ed. 57(2018) 4143-4148.
[7] J.B. Siegel, A. Zanghellini, H.M. Lovick, G. Kiss, A.R. Lambert, J.L.S. Clair, J.L. Gallaher, D. Hilvert, M.H. Gelb, B.L. Stoddard, K.N. Houk, F.E. Michael, D. Baker, Computational design of an enzyme catalyst for a stereoselective bimolecular diels-alder reaction, Science 329(2010) 309-313.
[8] L. Cao, Introduction:Immobilized enzymes:Past, present and prospects, Carrierbound Immobilized Enzymes, John Wiley & Sons, New Jersey, 2006.
[9] Y. Zhang, J. Ge, Z. Liu, Enhanced activity of immobilized or chemically modified enzymes, ACS Catal. 5(2015) 4503-4513.
[10] L. Cao, L. van Langen, R.A. Sheldon, Immobilised enzymes:Carrier-bound or carrier-free? Curr. Opin. Biotechnol. 14(2003) 387-394.
[11] R.A. Sheldon, S. van Pelt, Enzyme immobilisation in biocatalysis:Why, what and how, Chem. Soc. Rev. 42(2013) 6223-6235.
[12] L. Lancaster, W. Abdallah, S. Banta, I. Wheeldon, Engineering enzyme microenvironments for enhanced biocatalysis, Chem. Soc. Rev. 47(2018) 5177-5186.
[13] L. Goldstein, E. Katchalski, Use of water-insoluble enzyme derivatives in biochemical analysis and separation, Fresenius J. Anal. Chem. 243(1968) 375-396.
[14] B. Mattiasson, P. Aldercreutz, Tailoring the microenvironment of enzymes in water-poor systems, Trends Biotechnol. 9(1991) 394-398.
[15] Q. Jin, G. Jia, Y. Zhang, Q. Yang, C. Li, Hydrophobic surface induced activation of pseudomonas cepacia lipase immobilized into mesoporous silica, Langmuir 27(2011) 12016-12024.
[16] J.N. Vranish, M.G. Ancona, E. Oh, K. Susumu, I.L. Medintz, Enhancing coupled enzymatic activity by conjugating one enzyme to a nanoparticle, Nanoscale 9(2017) 5172-5187.
[17] W. Abdallah, K. Solanki, S. Banta, Insertion of a calcium-responsive beta-roll domain into a thermostable alcohol dehydrogenase enables tunable control over cofactor selectivity, ACS Catal. 8(2018) 1602-1613.
[18] M. Moniruzzaman, N. Kamiya, M. Goto, Activation and stabilization of enzymes in ionic liquids, Org. Biomol. Chem. 8(2010) 2887-2899.
[19] F. Secundo, Conformational changes of enzymes upon immobilisation, Chem. Soc. Rev. 42(2013) 6250-6261.
[20] D.R. Weilandt, V. Hatzimanikatis, Particle-based simulation reveals macromolecular crowding effects on the michaelis-menten mechanism, Biophys. J. 117(2019) 355-368.
[21] C. Balcells, I. Pastor, E. Vilaseca, S. Madurga, M. Cascante, F. Mas, Macromolecular crowding effect upon in vitro enzyme kinetics:Mixed activation-diffusion control of the oxidation of nadh by pyruvate catalyzed by lactate dehydrogenase, J. Phys. Chem. B 118(2014) 4062-4068.
[22] D. Homouz, M. Perham, A. Samiotakis, M.S. Cheung, P. Wittung-Stafshede, Crowded, cell-like environment induces shape changes in aspherical protein, Proc. Natl. Acad. Sci. U. S. A. 105(2008) 11754-11759.
[23] W. Wang, W.X. Xu, Y. Levy, E. Trizac, P.G. Wolynes, Confinement effects on the kinetics and thermodynamics of protein dimerization, Proc. Natl. Acad. Sci. U. S. A. 106(2009) 5517-5522.
[24] M. Senske, L. Tork, B. Born, M. Havenith, C. Herrmann, S. Ebbinghaus, Protein stabilization by macromolecular crowding through enthalpy rather than entropy, J. Am. Chem. Soc. 136(2014) 9036-9041.
[25] B.Y. Ma, R. Nussinov, Structured crowding and its effects on enzyme catalysis, Top. Curr. Chem. 337(2013) 123-137.
[26] Y. Levin, M. Pecht, L. Goldstein, E. Katchalski, A water-insoluble polyanionic derivative of trypsin. I. Preparation and properties, Biochemistry 3(1964) 1905-1913.
[27] H. Murata, C.S. Cummings, R.R. Koepsel, A.J. Russell, Rational tailoring of substrate and inhibitor affinity via atrp polymer-based protein engineering, Biomacromolecules 15(2014) 2817-2823.
[28] M. Cebula, I.S. Turan, B. Sjodin, M. Thulasingam, J. Brock, V. Chmyrov, J. Widengren, H. Abe, B. Mannervik, J.Z. Haeggstrom, A. Rinaldo-Matthis, E.U. Akkaya, R. Morgenstern, Catalytic conversion of lipophilic substrates by phase constrained enzymes in the aqueous or in the membrane phase, Sci. Rep. 6(2016) 38316.
[29] L. Goldstein, Y. Levin, E. Katchalski, A water-insoluble polyanionic derivative of trypsin. II. Effect of polyelectrolyte carrier on kinetic behavior of bound trypsin, Biochemistry 3(1964) 1913-1919.
[30] A. Harada, K. Kataoka, Pronounced activity of enzymes through the incorporation into the core of polyion complex micelles made from charged block copolymers, J. Control. Release 72(2001) 85-91.
[31] T. Kurinomaru, S. Tomita, Y. Hagihara, K. Shiraki, Enzyme hyperactivation system based on a complementary charged pair of polyelectrolytes and substrates, Langmuir 30(2014) 3826-3831.
[32] Y. Gao, C.C. Roberts, J. Zhu, J.L. Lin, C.E.A. Chang, I. Wheeldon, Tuning enzyme kinetics through designed intermolecular interactions far from the active site, ACS Catal. 5(2015) 2149-2153.
[33] Y. Azuma, D.L.V. Bader, D. Hilvert, Substrate sorting by a supercharged nanoreactor, J. Am. Chem. Soc. 140(2018) 860-863.
[34] L. Klermund, S.T. Poschenrieder, K. Castiglione, Biocatalysis in polymersomes:Improving multienzyme cascades with incompatible reaction steps by compartmentalization, ACS Catal. 7(2017) 3900-3904.
[35] Y.Liu,D.P.Hickey,J.Y.Guo, E. Earl,S.Abdellaoui,R.D.Milton,M.S.Sigman,S.D.Minteer, S.C. Barton, Substrate channeling in an artificial metabolon:A molecular dynamics blueprint for an experimental peptide bridge, ACS Catal. 7(2017) 2486-2493.
[36] J.L. Lin, I. Wheeldon, Kinetic enhancements in dna-enzyme nanostructures mimic the sabatier principle, ACS Catal. 3(2013) 560-564.
[37] A. Harada, K. Kataoka, Novel polyion complex micelles entrapping enzyme molecules in the core:Preparation of narrowly-distributed micelles from lysozyme and poly(ethylene glycol)-poly(aspartic acid) block copolymer in aqueous medium, Macromolecules 31(1998) 288-294.
[38] F. Caruso, D. Trau, H. Mohwald, R. Renneberg, Enzyme encapsulation in layer-bylayer engineered polymer multilayer capsules, Langmuir 16(2000) 1485-1488.
[39] M. Comellas-Aragones, H. Engelkamp, V.I. Claessen, N.A.J.M. Sommerdijk, A.E. Rowan, P.C.M. Christianen, J.C. Maan, B.J.M. Verduin, J.J.L.M. Cornelissen, R.J.M. Nolte, A virus-based single-enzyme nanoreactor, Nat. Nanotechnol. 2(2007) 635-639.
[40] P. Walde, Enzymatic reactions in liposomes, Curr. Opin. Colloid Interface Sci. 1(1996) 638-644.
[41] M. Nallani, H.P.M. de Hoog, J.J.L.M. Cornelissen, A.R.A. Palmans, J.C.M. van Hest, R.J.M. Nolte, Polymersome nanoreactors for enzymatic ring-opening polymerization, Biomacromolecules 8(2007) 3723-3728.
[42] T. Nishimura, K. Akiyoshi, Biotransporting biocatalytic reactors toward therapeutic nanofactories, Adv. Sci. 5(2018) 1800801.
[43] A. Kuchler, M. Yoshimoto, S. Luginbuhl, F. Mavelli, P. Walde, Enzymatic reactions in confined environments, Nat. Nanotechnol. 11(2016) 409-420.
[44] R. Chapman, M.H. Stenzel, All wrapped up:Stabilization of enzymes within single enzyme nanoparticles, J. Am. Chem. Soc. 141(2019) 2754-2769.
[45] T. Einfalt, D. Witzigmann, C. Edlinger, S. Sieber, R. Goers, A. Najer, M. Spulber, O. Onaca-Fischer, J. Huwyler, C.G. Palivan, Biomimetic artificial organelles with in vitro and in vivo activity triggered by reduction in microenvironment, Nat. Commun. 9(2018) 1127.
[46] S. Tsitkov, H. Hess, Design principles for a compartmentalized enzyme cascade reaction, ACS Catal. 9(2019) 2432-2439.
[47] M.T. Alam, V. Olin-Sandoval, A. Stincone, M.A. Keller, A. Zelezniak, B.F. Luisi, M. Ralser, The self-inhibitory nature of metabolic networks and its alleviation through compartmentalization, Nat. Commun. 8(2017) 16018.
[48] Y. Liu, I. Matanovic, D.P. Hickey, S.D. Minteer, P. Atanassov, S.C. Barton, Cascade kinetics of an artificial metabolon by molecular dynamics and kinetic Monte Carlo, ACS Catal. 8(2018) 7719-7726.
[49] Y. Liu, D.P. Hickey, S.D. Minteer, A. Dickson, S.C. Barton, Markov-state transition path analysis of electrostatic channeling, J. Phys. Chem. C 123(2019) 15284-15292.
[50] M. Yoshimoto, Stabilization of enzymes through encapsulation in liposomes, Methods Mol. Biol. 1504(2017) 9-18.
[51] S. Besic, S.D. Minteer, Micellar polymer encapsulation of enzymes, Methods Mol. Biol. 1504(2017) 93-108.
[52] X. Lian, A. Erazo-Oliveras, J.P. Pellois, H.C. Zhou, High efficiency and long-term intracellular activity of an enzymatic nanofactory based on metal-organic frameworks, Nat. Commun. 8(2017) 2075.
[53] Z. Zhao, J. Fu, S. Dhakal, A. Johnson-Buck, M. Liu, T. Zhang, N.W. Woodbury, Y. Liu, N.G. Walter, H. Yan, Nanocaged enzymes with enhanced catalytic activity and increased stability against protease digestion, Nat. Commun. 7(2016) 10619.
[54] Y. Liu, J. Du, M. Yan, M.Y. Lau, J. Hu, H. Han, O.O. Yang, S. Liang, W. Wei, H. Wang, J.M. Li, X.Y. Zhu, L. Shi, W. Chen, C. Ji, Y. Lu, Biomimetic enzyme nanocomplexes and their use as antidotes and preventive measures for alcohol intoxication, Nat. Nanotechnol. 8(2013) 187-192.
[55] X. Wu, H. Yue, Y. Zhang, X. Gao, X. Li, L. Wang, Y. Cao, M. Hou, H. An, L. Zhang, S. Li, J. Ma, H. Lin, Y. Fu, H. Gu, W. Lou, W. Wei, R.N. Zare, J. Ge, Packaging and delivering enzymes by amorphous metal-organic frameworks, Nat. Commun. 10(2019) 5165.
[56] V. Leskovac, The pH Dependence of Enzyme Catalysis. In:Comprehensive Enzyme Kinetics, Springer, Boston, MA, 2004, 283-315.
[57] A. Nakamura, K. Haga, K. Yamane, Three histidine-residues in the active-center of cyclodextrin glucanotransferase from alkalophilic bacillus sp-1011:Effects of the replacement on pH-dependence and transition-state stabilization, Biochemistry 32(1993) 6624-6631.
[58] J.N. Rodriguez-Lopez, D.J. Lowe, J. Hernandez-Ruiz, A.N.P. Hiner, F. Garcia-Canovas, R.N.F. Thorneley, Mechanism of reaction of hydrogen peroxide with horseradish peroxidase:Identification of intermediates in the catalytic cycle, J. Am. Chem. Soc. 123(2001) 11838-11847.
[59] L. Goldstein, Microenvironmental effects on enzyme catalysis-kinetic study of polyanionic and polycationic derivatives of chymotrypsin, Biochemistry 11(1972) 4072-4084.
[60] Y. Zhang, Q. Wang, H. Hess, Increasing enzyme cascade throughput by phengineering the microenvironment of individual enzymes, ACS Catal. 7(2017) 2047-2051.
[61] H. Suzuki, Y. Ozawa, H. Maeda, Studies on water-insoluble enzyme hydrolysis of sucrose by insoluble yeast invertase, Agric. Biol. Chem. 30(1966) 807-812.
[62] E. Biro, A.S. Nemeth, C. Sisak, J. Gyemis, B. Szajani, Beta-galactosidase immobilization on chitosan microspheres, J. Biotechnol. 131(2007) S98.
[63] D. Yang, J.H. Fan, F.Y. Cao, Z.J. Deng, J.A. Pojman, L. Ji, Immobilization adjusted clock reaction in the urea-urease-H⁺ reaction system, RSC Adv. 9(2019) 3514-3519.
[64] R.A. Zingaro, M. Uziel, Preparation and properties of active, insoluble alkaline phosphatase, Biochim. Biophys. Acta 213(1970) 371-379.
[65] J. Müller, C.M. Niemeyer, DNA-directed assembly of artificial multienzyme complexes, Biochem. Biophys. Res. Commun. 377(2008) 62-67.
[66] O.I. Wilner, Y. Weizmann, R. Gill, O. Lioubashevski, R. Freeman, I. Willner, Enzyme cascades activated on topologically programmed DNA scaffolds, Nat. Nanotechnol. 4(2009) 249-254.
[67] J. Fu, M. Liu, Y. Liu, N.W. Woodbury, H. Yan, Interenzyme substrate diffusion for an enzyme cascade organized on spatially addressable DNA nanostructures, J. Am. Chem. Soc. 134(2012) 5516-5519.
[68] L. Xin, C. Zhou, Z. Yang, D. Liu, Regulation of an enzyme cascade reaction by a DNA machine, Small 9(2013) 3088-3091.
[69] C. You, S. Myung, Y.H.P. Zhang, Facilitated substrate channeling in a self-assembled trifunctional enzyme complex, Angew. Chem. Int. Ed. 51(2012) 8787-8790.
[70] C. You, Y.H.P. Zhang, Self-assembly of synthetic metabolons through synthetic protein scaffolds:One-step purification, co-immobilization, and substrate channeling, ACS Synth. Biol. 2(2013) 102-110.
[71] O. Idan, H. Hess, Origins of activity enhancement in enzyme cascades on scaffolds, ACS Nano 7(2013) 8658-8665.
[72] Y. Zhang, S. Tsitkov, H. Hess, Proximity does not contribute to activity enhancement in the glucose oxidase-horseradish peroxidase cascade, Nat. Commun. 13982(2016).
[73] Y. Zhang, H. Hess, Toward rational design of high-efficiency enzyme cascades, ACS Catal. 7(2017) 6018-6027.
[74] K.S. Rabe, J. Muller, M. Skoupi, C.M. Niemeyer, Cascades in compartments:En route to machine-assisted biotechnology, Angew. Chem. Int. Ed. 56(2017) 13574-13589.
[75] L.J. Sweetlove, A.R. Fernie, The role of dynamic enzyme assemblies and substrate channelling in metabolic regulation, Nat. Commun. 9(2018) 2136.
[76] C. Eun, P.M. Kekenes-Huskey, V.T. Metzger,J.A.McCammon, A model study of sequential enzyme reactions and electrostatic channeling, J. Chem. Phys. 140(2014) 105101.
[77] A. Kuzmak, S. Carmali, E. von Lieres, A.J. Russell, S. Kondrat, Can enzyme proximity accelerate cascade reactions? Sci. Rep. 9(2019) 455.
[78] I. Wheeldon, S.D. Minteer, S. Banta, S.C. Barton, P. Atanassov, M. Sigman, Substrate channelling as an approach to cascade reactions, Nat. Chem. 8(2016) 299-309.
[79] T. Obata, Toward an evaluation of metabolite channeling in vivo, Curr. Opin. Biotechnol. 64(2020) 55-61.
[80] H.O. Spivey, J. Ovadi, Substrate channeling, Methods 19(1999) 306-321.
[81] V. Linko, M. Eerikainen, M.A. Kostiainen, A modular DNA origami-based enzyme cascade nanoreactor, Chem. Commun. 51(2015) 5351-5354.
[82] J. Collins, T. Zhang, S.W. Oh, R. Maloney, J. Fu, DNA-crowded enzyme complexes with enhanced activities and stabilities, Chem. Commun. 53(2017) 13059-13062.
[83] A.M. Klibanov, Improving enzymes by using them in organic solvents, Nature 409(2001) 241-246.
[84] S.V. Kamat, E.J. Beckman, A.J. Russell, Enzyme activity in supercritical fluids, Crit. Rev. Biotechnol. 15(1995) 41-71.
[85] E. Barzana, A.M. Klibanov, M. Karel, Enzyme-catalyzed, gas-phase reactions, Appl. Biochem. Biotechnol. 15(1987) 25-34.
[86] P.J. Halling, Rates of enzymic reactions in predominantly organic, low water systems, Biocatalysis 1(1987) 109-115.
[87] A. Zaks, A.M. Klibanov, Enzyme-catalyzed processes in organic solvents, Proc. Natl. Acad. Sci. U. S. A. 82(1985) 3192-3196.
[88] M.N. Gupta, Enzyme function in organic solvents, Eur. J. Biochem. 203(1992) 25-32.
[89] M. Tarek, D.J. Tobias, The dynamics of protein hydration water:A quantitative comparison of molecular dynamics simulations and neutron-scattering experiments, Biophys. J. 79(2000) 3244-3257.
[90] P.J. Haring, What can we learn by studying enzymes in non-aqueous media? Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 359(2004) 1287-1296.
[91] L. Yang, J.S. Dordick, S. Garde, Hydration of enzyme in nonaqueous media is consistent with solvent dependence of its activity, Biophys. J. 87(2004) 812-821.
[92] N.M. Micaelo, C.M. Soares, Modeling hydration mechanisms of enzymes in nonpolar and polar organic solvents, FEBS J. 274(2007) 2424-2436.
[93] A. Zaks, A.M. Klibanov, Enzymatic catalysis in nonaqueous solvents, J. Biol. Chem. 263(1988) 3194-3201.
[94] L. Dai, A.M. Klibanov, Striking activation of oxidative enzymes suspended in nonaqueous media, Proc. Natl. Acad. Sci. U. S. A. 96(1999) 9475-9478.
[95] N. Bruns, J.C. Tiller, Amphiphilic network as nanoreactor for enzymes in organic solvents, Nano Lett. 5(2005) 45-48.
[96] M. Yan, J. Ge, Z. Liu, P. Ouyang, Encapsulation of single enzyme in nanogel with enhanced biocatalytic activity and stability, J. Am. Chem. Soc. 128(2006) 11008-11009.
[97] J. Ge, D. Lu, J. Wang, Z. Liu, Lipase nanogel catalyzed transesterification in anhydrous dimethyl sulfoxide, Biomacromolecules 10(2009) 1612-1618.
[98] S. Badieyan, Q. Wang, X. Zou, Y. Li, M. Herron, N.L. Abbott, Z. Chen, E.N.G. Marsh, Engineered surface-immobilized enzyme that retains high levels of catalytic activity in air, J. Am. Chem. Soc. 139(2017) 2872-2875.
[99] J. Ge, D. Lu, J. Wang, M. Yan, Y. Lu, Z. Liu, Molecular fundamentals of enzyme nanogels, J. Phys. Chem. B 112(2008) 14319-14324.
[100] K. Kimura, A. Suzuki, H. Inokuchi, T. Yagi, Hydrogenase activity in the dry state:Isotope exchange and reversible oxidoreduction of cytochrome-c3, Biochim. Biophys. Acta 567(1979) 96-105.
[101] R.V. Dunn, R.M. Daniel, The use of gas-phase substrates to study enzyme catalysis at low hydration, Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 359(2004) 1309-1320.
[102] V. Kurkal, R.M. Daniel, J.L. Finney, M. Tehei, R.V. Dunn, J.C. Smith, Enzyme activity and flexibility at very low hydration, Biophys. J. 89(2005) 1282-1287.
[103] K. Nagayama, A.C. Spiess, J. Buchs, Enhanced catalytic performance of immobilized Parvibaculum lavamentivorans alcohol dehydrogenase in a gas phase bioreactor using glycerol as an additive, Chem. Eng. J. 207(2012) 342-348.
[104] A.H. Trivedi, A.C. Spiess, T. Daussmann, J. Büchs, Effect of additives on gas-phase catalysis with immobilised Thermoanaerobacter species alcohol dehydrogenase (ADH T), Appl. Microbiol. Biotechnol. 71(2006) 407-414.
[105] A.W. Perriman, H. Colfen, R.W. Hughes, C.L. Barrie, S. Mann, Solvent-free protein liquids and liquid crystals, Angew. Chem. Int. Ed. 48(2009) 6242-6246.
[106] A.P.S. Brogan, R.B. Sessions, A.W. Perriman, S. Mann, Molecular dynamics simulations reveal a dielectric-responsive coronal structure in protein-polymer surfactant hybrid nanoconstructs, J. Am. Chem. Soc. 136(2014) 16824-16831.
[107] A.W. Perriman, S. Mann, Liquid proteins-a new frontier for biomolecule-based nanoscience, ACS Nano 5(2011) 6085-6091.
[108] W. Xu, Z. Fu, G. Chen, Z. Wang, Y. Jian, Y. Zhang, G. Jiang, D. Lu, J. Wu, Z. Liu, Graphene oxide enabled long-term enzymatic transesterification in an anhydrous gas flux, Nat. Commun. 10(2019) 2684.
[109] Z. Fu, W. Xu, G. Chen, Z. Wang, D. Lu, J. Wu, Z. Liu, Molecular dynamics simulations reveal how graphene oxide stabilizes and activates lipase in an anhydrous gas, Phys. Chem. Chem. Phys. 21(2019) 25425-25430.
[110] Z. Sun, Q. Liu, G. Qu, Y. Feng, M.T. Reetz, Utility of B-factors in protein science:Interpreting rigidity, flexibility, and internal motion and engineering thermostability, Chem. Rev. 119(2019) 1626-1665.
[111] R.M. Daniel, M.J. Danson, Temperature and the catalytic activity of enzymes:A fresh understanding, FEBS Lett. 587(2013) 2738-2743.
[112] M.D. Blankschien, L.A. Pretzer, R. Huschka, N.J. Halas, R. Gonzalez, M.S. Wong, Light-triggered biocatalysis using thermophilic enzyme-gold nanoparticle complexes, ACS Nano 7(2013) 654-663.
[113] C. Wang, Q. Zhang, X. Wang, H. Chang, S. Zhang, Y. Tang, J. Xu, R. Qi, Y. Cheng, Dynamic modulation of enzyme activity by near-infrared light, Angew. Chem. Int. Ed. 56(2017) 6767-6772.
[114] S. Zhang, C. Wang, H. Chang, Q. Zhang, Y. Cheng, Off-on switching of enzyme activity by near-infrared light-induced photothermal phase transition of nanohybrids, Sci. Adv. 5(2019) eaaw4252.
[115] A. Rajabpour, R. Seif, S. Arabha, M.M. Heyhat, S. Merabia, A. Hassanali, Thermal transport at a nanoparticle-water interface:A molecular dynamics and continuum modeling study, J. Chem. Phys. 150(2019) 114701.
[116] K.M. Hoogeboom-Pot, J.N. Hernandez-Charpak, X. Gu, T.D. Frazer, E.H. Anderson, W. Chao, R.W. Falcone, R. Yang, M.M. Murnane, H.C. Kapteyn, D. Nardi, A new regime of nanoscale thermal transport:Collective diffusion increases dissipation efficiency, Proc. Natl. Acad. Sci. U. S. A. 112(2015) 4846-4851.
[117] S. Maity, W.C. Wu, J.B. Tracy, L.I. Clarke, J.R. Bochinski, Nanoscale steady-state temperature gradients within polymer nanocomposites undergoing continuous-wave photothermal heating from gold nanorods, Nanoscale 9(2017) 11605-11618.