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Review Articles

Enzymatic regeneration and conservation of ATP: challenges and opportunities

ORCID Icon & ORCID Icon
Pages 16-33 | Received 19 Mar 2020, Accepted 30 Aug 2020, Published online: 04 Oct 2020

References

  • Hollenstein K, Dawson RJP, Locher KP. Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol. 2007;17(4):412–418.
  • Kitao A, Hata H. Molecular dynamics simulation of bacterial flagella. Biophys Rev. 2018;10(2):617–629.
  • Sweeney HL, Houdusse A. Structural and functional insights into the myosin motor mechanism. Annu Rev Biophys. 2010;39(1):539–557.
  • Huang R, Chen H, Upp DM, et al. A high-throughput method for directed evolution of NAD(P)+-dependent dehydrogenases for the reduction of biomimetic nicotinamide analogues. ACS Catal. 2019;9(12):11709–11719.,
  • Nelson DL, Cox MM. 2008. Lehninger principles of biochemistry. 5th ed. New York: WH Freeman.
  • Lian Q, Cao H, Wang F. The cost-efficiency realization in the Escherichia coli-based cell-free protein synthesis systems. Appl Biochem Biotechnol. 2014;174(7):2351–2367.
  • Corriden R, Insel PA. Basal release of ATP: an autocrine-paracrine mechanism for cell regulation. Sci Signal. 2010;3(104):re1.
  • Praetorius HA, Leipziger J. Intrarenal purinergic signaling in the control of renal tubular transport. Annu Rev Physiol. 2010;72(1):377–393.
  • Bos JL. Epac proteins: multi-purpose cAMP targets. Trends Biochem Sci. 2006;31(12):680–686.
  • Berg JM, Tymoczko JL, Stryer L. 2002. Biochemistry. 5th ed. New York: W. H. Freeman & Co.
  • Jia Y, Li J. Reconstitution of FoF1-ATPase-based biomimetic systems. Nat Rev Chem. 2019;3(6):361–374.
  • Junge W, Nelson N. ATP Synthase. Annu Rev Biochem. 2015;84(1):631–657.
  • Baker JS, McCormick MC, Robergs RA. Interaction among skeletal muscle metabolic energy systems during intense exercise. J Nutr Metab. 2010;2010:905612–905612.
  • Shi T, Han P, You C, et al. An in vitro synthetic biology platform for emerging industrial biomanufacturing: bottom-up pathway design . Synth Syst Biotechnol. 2018;3(3):186–195.
  • Demain AL. The business of biotechnology. Ind Biotechnol. 2007;3(3):269–283.
  • Vogel A, May O. 2019. Industrial enzyme applications. Weinheim (Germany): Wiley-VCH.
  • Zhang Y-HP. Production of biocommodities and bioelectricity by cell-free synthetic enzymatic pathway biotransformations: challenges and opportunities. Biotechnol Bioeng. 2010;105(4):663–677.
  • Opgenorth PH, Korman TP, Bowie JU. A synthetic biochemistry molecular purge valve module that maintains redox balance. Nat Commun. 2014;5:4113.
  • Sperl JM, Sieber V. Multienzyme cascade reactions—status and recent advances. ACS Catal. 2018;8(3):2385–2396.
  • Taniguchi H, Okano K, Honda K. Modules for in vitro metabolic engineering: Pathway assembly for bio-based production of value-added chemicals. Synth Syst Biotechnol. 2017;2(2):65–74.
  • Zhang Y-HP. Production of biofuels and biochemicals by in vitro synthetic biosystems: Opportunities and challenges. Biotechnol Adv. 2015;33(7):1467–1483.
  • Fujisawa T, Fujinaga S, Atomi H. An in vitro enzyme system for the production of myo-inositol from starch. Appl Environ Microbiol. 2017;83(16):e00550–e00517.
  • You C, Shi T, Li Y, et al. An in vitro synthetic biology platform for the industrial biomanufacturing of myo-inositol from starch. Biotechnol Bioeng. 2017;114(8):1855–1864.
  • Zhao H, van der Donk WA. Regeneration of cofactors for use in biocatalysis. Curr Opin Biotechnol. 2003;14(6):583–589.
  • Andexer JN, Richter M. Emerging enzymes for ATP regeneration in biocatalytic processes. Chembiochem. 2015;16(3):380–386.
  • Kim D-M, Swartz JR. Prolonging cell-free protein synthesis with a novel ATP regeneration system. Biotechnol Bioeng. 1999;66(3):180–188.
  • Wei X, Xie L, Job Zhang Y-HP, et al. Stoichiometric regeneration of ATP by a NAD(P)/CoA-free and phosphate-balanced in vitro synthetic enzymatic biosystem. ChemCatChem. 2018;10(24):5597–5601.
  • Zhang J, Wu B, Zhang Y, et al. Creatine phosphate-creatine kinase in enzymatic synthesis of glycoconjugates. Org Lett. 2003;5(15):2583–2586.
  • Baughn RL, Adalsteinsson O, Whitesides GM. Large-scale enzyme-catalyzed synthesis of ATP from adenosine and acetyl phosphate: Regeneration of ATP from AMP. J Am Chem Soc. 1978;100(1):304–306.
  • Mordhorst S, Siegrist J, Müller M, et al. Catalytic alkylation using a cyclic S-adenosylmethionine regeneration system. Angew Chem Int Ed Engl. 2017b;56(14):4037–4041.
  • Zhao A, Ding R, Zhai M. Multi-enzymatic recycling of ATP and NADPH for the synthesis of 5-aminolevulinic acid using a semipermeable reaction system. Biosci Biotechnol Biochem. 2019;83:2213–2219.
  • Tasnádi G, Jud W, Hall M, et al. Evaluation of natural and synthetic phosphate donors for the improved enzymatic synthesis of phosphate monoesters. Adv Synth Catal. 2018;360(12):2394–2401.
  • Huffman MA, Fryszkowska A, Alvizo O, et al. Design of an in vitro biocatalytic cascade for the manufacture of islatravir. Science. 2019;366(6470):1255–1259.
  • Velasquez JE, Green PR, Wos JA. 2015. Method for preparing nicotinamide riboside. US20170121746A1.
  • Brown MR, Kornberg A. Inorganic polyphosphate in the origin and survival of species. Proc Natl Acad Sci Usa. 2004;101(46):16085–16087.
  • Honda K, Hara N, Cheng M, et al. In vitro metabolic engineering for the salvage synthesis of NAD(+). Metab Eng. 2016;35:114–120.
  • Hirota R, Kuroda A, Kato J, et al. Bacterial phosphate metabolism and its application to phosphorus recovery and industrial bioprocesses. J Biosci Bioeng. 2010;109(5):423–432.
  • Matsumiya Y, Yamasita T, Nawamura Y. Phosphorus removal from sidestreams by crystallisation of magnesium-ammonium-phosphate using seawater. Water Environ J. 2000;14(4):291–296.
  • Wang L, Yan J, Wise MJ, et al. Distribution patterns of polyphosphate metabolism pathway and its relationships with bacterial durability and virulence. Front Microbiol. 2018;9:782. (
  • Motomura K, Hirota R, Okada M, et al. A new subfamily of polyphosphate kinase 2 (class III PPK2) catalyzes both nucleoside monophosphate phosphorylation and nucleoside diphosphate phosphorylation. Appl Environ Microbiol. 2014;80(8):2602–2608.
  • Akiyama M, Crooke E, Kornberg A. The polyphosphate kinase gene of Escherichia coli. isolation and sequence of the ppk gene and membrane location of the protein. J Biol Chem. 1992;267(31):22556–22561.
  • Tzeng C-M, Kornberg A. The multiple activities of polyphosphate kinase of Escherichia coli and their subunit structure determined by radiation target analysis. J Biol Chem. 2000;275(6):3977–3983.
  • Zhu Y, Huang W, Lee SSK, et al. Crystal structure of a polyphosphate kinase and its implications for polyphosphate synthesis. EMBO Rep. 2005;6(7):681–687.
  • Murata K, Uchida T, Kato J, et al. Polyphosphate kinase: distribution, some properties and its application as an ATP regeneration system. Agri Biol Chem. 1988;52(6):1471–1477.
  • Shimane M, Sugai Y, Kainuma R, et al. Mevalonate-dependent enzymatic synthesis of amorphadiene driven by an ATP-regeneration system using polyphosphate kinase. Biosci Biotechnol Biochem. 2012;76(8):1558–1560.
  • Meng Q, Zhang Y, Ju X, et al. Production of 5-aminolevulinic acid by cell free multi-enzyme catalysis. J Biotechnol. 2016;226:8–13.
  • Noguchi T, Shiba T. Use of Escherichia coli polyphosphate kinase for oligosaccharide synthesis. Biosci Biotechnol Biochem. 1998;62(8):1594–1596.
  • Iwamoto S, Motomura K, Shinoda Y, et al. Use of an Escherichia coli recombinant producing thermostable polyphosphate kinase as an ATP regenerator to produce fructose 1,6-diphosphate. Appl Environ Microbiol. 2007;73(17):5676–5678.
  • Honda K, Maya S, Omasa T, et al. Production of 2-deoxyribose 5-phosphate from fructose to demonstrate a potential of artificial bio-synthetic pathway using thermophilic enzymes. J Biotechnol. 2010;148(4):204–207.
  • Restiawaty E, Iwasa Y, Maya S, et al. Feasibility of thermophilic adenosine triphosphate-regeneration system using Thermus thermophilus polyphosphate kinase. Process Biochem. 2011;46(9):1747–1752.
  • Restiawaty E, Honda K, Okano K, et al. Construction of membrane-anchoring fusion protein of Thermococcus kodakaraensis glycerol kinase and its application to repetitive batchwise reactions. J Biosci Bioeng. 2012;113(4):521–525.
  • Kim J-E, Zhang Y-HP. Biosynthesis of D-xylulose 5-phosphate from D-xylose and polyphosphate through a minimized two-enzyme cascade. Biotechnol Bioeng. 2016;113(2):275–282.
  • Honda K, Kimura K, Ninh PH, et al. In vitro bioconversion of chitin to pyruvate with thermophilic enzymes. J Biosci Bioeng. 2017;124(3):296–301.
  • Sato M, Masuda Y, Kirimura K, et al. Thermostable ATP regeneration system using polyphosphate kinase from Thermosynechococcus elongatus BP-1 for D-amino acid dipeptide synthesis. J Biosci Bioeng. 2007;103(2):179–184.
  • Zhang X, Wu H, Huang B, et al. One-pot synthesis of glutathione by a two-enzyme cascade using a thermophilic ATP regeneration system. J Biotechnol. 2017;241:163–169.
  • Mordhorst S, Maurer A, Popadić D, et al. A flexible polyphosphate-driven regeneration system for coenzyme A dependent catalysis. ChemCatChem. 2017a;9(22):4164–4168.
  • Strohmeier GA, Eiteljörg IC, Schwarz A, et al. Enzymatic one-step reduction of carboxylates to aldehydes with cell-free regeneration of ATP and NADPH. Chemistry. 2019;25(24):6119–6123.
  • Strohmeier GA, Schwarz A, Andexer JN, et al. Co-factor demand and regeneration in the enzymatic one-step reduction of carboxylates to aldehydes in cell-free systems. J Biotechnol. 2020;307:202–207.
  • Cao H, Li C, Zhao J, et al. Enzymatic production of glutathione coupling with an ATP regeneration system based on polyphosphate kinase. Appl Biochem Biotechnol. 2018;185(2):385–395.
  • Li Y, Liu S, Zhu J. Construction of recombinant strains co-expressing PPK and GMAS for the synthesis of L-theanine. Chin. J. Biotechnol. 2016;32:1745–1749.
  • Liu S, Li Y, Zhu J. Enzymatic production of l-theanine by γ-glutamylmethylamide synthetase coupling with an ATP regeneration system based on polyphosphate kinase. Proc Biochem. 2016;51(10):1458–1463.
  • Kulmer ST, Gutmann A, Lemmerer M, et al. Biocatalytic cascade of polyphosphate kinase and sucrose synthase for synthesis of nucleotide-activated derivatives of glucose. Adv Synth Catal. 2017;359(2):292–301.
  • Suzuki S, Hara R, Kino K. Production of aminoacyl prolines using the adenylation domain of nonribosomal peptide synthetase with class III polyphosphate kinase 2-mediated ATP regeneration. J Biosci Bioeng. 2018;125(6):644–648.
  • Hrabárová E, Achbergerová L, Nahálka J. Insoluble protein applications: The use of bacterial inclusion bodies as biocatalysts. In: García-Fruitós E, editor. Insoluble proteins: methods and protocols. New York (NY): Springer; 2015. p. 411–422.
  • Ishige K, Zhang H, Kornberg A. Polyphosphate kinase (PPK2), a potent, polyphosphate-driven generator of GTP. Proc Natl Acad Sci USA. 2002;99(26):16684–16688.
  • Zhang H, Ishige K, Kornberg A. A polyphosphate kinase (PPK2) widely conserved in bacteria. Proc Natl Acad Sci USA. 2002;99(26):16678–16683.
  • Nocek B, Kochinyan S, Proudfoot M, et al. Polyphosphate-dependent synthesis of ATP and ADP by the family-2 polyphosphate kinases in bacteria. Proc Natl Acad Sci USA. 2008;105(46):17730–17735.
  • Zhang X, Cui X, Shen S, et al. Engineering of supramolecular nanoreactors by assembly of multiple enzymes for ATP regeneration in vitro. Biochem Eng J. 2020b;155:107487.
  • Mordhorst S, Singh J, Mohr MKF, et al. Several polyphosphate Kinase 2 enzymes catalyse the production of adenosine 5'-polyphosphates. Chembiochem. 2019;20(8):1019–1022.
  • Zhang X, Cui X, Li Z. Characterization of two polyphosphate kinase 2 enzymes used for ATP synthesis. Appl Biochem Biotechnol. 2020a;191:881–892.
  • Ogawa M, Uyeda A, Harada K, et al. Class III polyphosphate kinase 2 enzymes catalyze the pyrophosphorylation of adenosine-5'-monophosphate. Chembiochem. 2019;20(23):2961–2967.
  • Resnick SM, Zehnder AJ. In vitro ATP regeneration from polyphosphate and AMP by polyphosphate:AMP phosphotransferase and adenylate kinase from Acinetobacter johnsonii 210A. Appl Environ Microbiol. 2000;66(5):2045–2051.
  • Sommer-Kamann C, Fries A, Mordhorst S, et al. Asymmetric C-alkylation by the S-adenosylmethionine-dependent methyltransferase SgvM. Angew Chem Int Ed Engl. 2017;56(14):4033–4036.
  • Carlson ED, Gan R, Hodgman CE, et al. Cell-free protein synthesis: applications come of age. Biotechnol Adv. 2012;30(5):1185–1194.
  • Pardee K, Slomovic S, Nguyen PQ, et al. Portable, on-demand biomolecular manufacturing. Cell. 2016;167(1):248–259.e212.
  • Jewett MC, Swartz JR. Mimicking the Escherichia coli cytoplasmic environment activates long-lived and efficient cell-free protein synthesis. Biotechnol Bioeng. 2004;86(1):19–26.
  • Wang Y, Zhang Y-HP. Cell-free protein synthesis energized by slowly-metabolized maltodextrin. BMC Biotechnol. 2009;9:58.
  • Kim D-M, Swartz JR. Regeneration of adenosine triphosphate from glycolytic intermediates for cell-free protein synthesis. Biotechnol Bioeng. 2001;74(4):309–316.
  • Calhoun KA, Swartz JR. Energizing cell-free protein synthesis with glucose metabolism. Biotechnol Bioeng. 2005;90(5):606–613.
  • Kim H-C, Kim T-W, Park C-G, et al. Continuous cell-free protein synthesis using glycolytic intermediates as energy sources. J Microbiol Biotechnol. 2008;18(5):885–888.
  • Caschera F, Noireaux V. A cost-effective polyphosphate-based metabolism fuels an all E. coli cell-free expression system. Metab Eng. 2015;27:29–37.
  • Mueller-Langer F, Tzimas E, Kaltschmitt M, et al. Techno-economic assessment of hydrogen production processes for the hydrogen economy for the short and medium term. Int J Hydrogen Energy. 2007;32(16):3797–3810.
  • Suraniti E, Merzeau P, Roche J, et al. Uphill production of dihydrogen by enzymatic oxidation of glucose without an external energy source. Nat Commun. 2018;9(1):3229.
  • Thauer K, Jungermann K, Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977;41(1):100–180.
  • Woodward J, Orr M, Cordray K, et al. Enzymatic production of biohydrogen. Nature. 2000;405(6790):1014–1015.
  • Zhang Y-HP, Evans BR, Mielenz JR, et al. High-yield hydrogen production from starch and water by a synthetic enzymatic pathway. PLoS One. 2007;2(5):e456
  • Zhang YHP, Mielenz J. 2006. Biohydrogen production by an artificial enzymatic pathway. US 8,211,681. Google Patents.
  • Kim J-E, Kim E-J, Chen H, et al. Advanced water splitting for green hydrogen gas production through complete oxidation of starch by in vitro metabolic engineering. Metab Eng. 2017;44:246–252.
  • Kim E-J, Kim J-E, Zhang Y-HPJ. Ultra-rapid rates of water splitting for biohydrogen gas production through in vitro artificial enzymatic pathways. Energy Environ Sci. 2018;11(8):2064–2072.
  • Kim E-J, Adams M, Wu C-H, et al. Exceptionally high rates of biological hydrogen production by biomimetic in vitro synthetic enzymatic pathways. Chemistry. 2016;22(45):16047–16051.
  • Chen H, Huang R, Kim E-J, et al. Building a thermostable metabolon for facilitating coenzyme transport and in vitro hydrogen production at elevated temperature. ChemSusChem. 2018;11(18):3120–3030.
  • Myung S, Rollin J, You C, et al. In vitro metabolic engineering of hydrogen production at theoretical yield from sucrose. Metab Eng. 2014;24:70–77.
  • Ye X, Wang Y, Hopkins RC, et al. Spontaneous high-yield production of hydrogen from cellulosic materials and water catalyzed by enzyme cocktails. ChemSusChem. 2009;2(2):149–152.
  • del Campo M, Rollin JS, Myung J, et al. High-yield production of dihydrogen from xylose by using a synthetic enzyme cascade in a cell-free system. Angew Chem Int Ed Engl. 2013;52(17):4587–4590.
  • Rollin JA, Martin del Campo J, Myung S, et al. High-yield hydrogen production from biomass by in vitro metabolic engineering: mixed sugars coutilization and kinetic modeling. Proc Natl Acad Sci Usa. 2015;112(16):4964–4969.
  • Moustafa HMA, Kim E-J, Zhu Z, et al. Water splitting for high-yield hydrogen production energized by biomass xylooligosaccharides catalyzed by an enzyme cocktail. ChemCatChem. 2016;8(18):2898–2902.
  • Zhou W, Huang R, Zhu Z, et al. Coevolution of both thermostability and activity of polyphosphate glucokinase from Thermobifida fusca YX. Appl Environ Microbiol. 2018;84(16):e01224-18.
  • Guterl J-K, Garbe D, Carsten J, et al. Cell-free metabolic engineering: production of chemicals by minimized reaction cascades. ChemSusChem. 2012;5(11):2165–2172.
  • Xie L, Wei X, Zhou X, et al. Conversion of D-glucose to L-lactate via pyruvate by an optimized cell-free enzymatic biosystem containing minimized reactions. Synth Syst Biotechnol. 2018;3(3):204–210.
  • Okano K, Zhu Q, Honda K. In vitro reconstitution of non-phosphorylative Entner–Doudoroff pathway for lactate production. J Biosci Bioeng. 2020;129:269–275. doi.org/10.1016/j.jbiosc.2019.1009.1010.
  • Granström TB, Takata G, Tokuda M, et al. Izumoring: a novel and complete strategy for bioproduction of rare sugars. J Biosci Bioeng. 2004;97(2):89–94.
  • Yang J, Zhang T, Tian C, et al. Multi-enzyme systems and recombinant cells for synthesis of valuable saccharides: advances and perspectives. Biotechnol Adv. 2019;37(7):107406.
  • Wen L, Huang K, Wei M, et al. Facile enzymatic synthesis of ketoses. Angew Chem Int Ed Engl. 2015;54(43):12654–12658.
  • Liao HH, Myung S, Zhang Y-HP. One-step purification and immobilization of thermophilic polyphosphate glucokinase from Thermobifida fusca YX: glucose-6-phosphate generation without ATP. Appl Microbiol Biotechnol. 2012;93(3):1109–1117.
  • Lu Y, Wang L, Teng F, et al. Production of myo-inositol from glucose by a novel trienzymatic cascade of polyphosphate glucokinase, inositol 1-phosphate synthase and inositol monophosphatase. Enzyme Microb Technol. 2018;112:1–5.
  • Cheng K, Zheng W, Chen H, et al. Upgrade of wood sugar D-xylose to a value-added nutraceutical by in vitro metabolic engineering. Metab Eng. 2019;52:1–8.
  • Zhong C, You C, Wei P, et al. Thermal cycling cascade biocatalysis of myo-inositol synthesis from sucrose. ACS Catal. 2017;7(9):5992–5999.
  • Bai X, Meng D, Wei X, et al. Facile synthesis of (-)-vibo-quercitol from maltodextrin via an in vitro synthetic enzymatic biosystem . Biotechnol Bioeng. 2019;116(10):2710–2719.
  • Wang W, Liu M, You C, et al. ATP-free biosynthesis of a high-energy phosphate metabolite fructose 1,6-diphosphate by in vitro metabolic engineering. Metab Eng. 2017;42:168–174.
  • Wang W, Yang J, Sun Y, et al. Artificial ATP-free in vitro synthetic enzymatic biosystems facilitate aldolase-mediated C–C bond formation for biomanufacturing. ACS Catal. 2020;10(2):1264–1271.
  • Widjaja A, Shiroshima M, Yasuda M, et al. Enzymatic synthesis of fructose 1,6-Diphosphate with ATP regeneration in a batch reactor and a semibatch reactor using purified enzymes of Bacillus stearothermophilus. J Biosci Bioeng. 1999;87(5):611–618.
  • Xiao X, Xia H-q, Wu R, et al. Tackling the challenges of enzymatic (bio)fuel cells. Chem Rev. 2019;119(16):9509–9558.
  • Zhu Z-G, Kin Tam T, Sun F, et al. A high-energy-density sugar biobattery based on a synthetic enzymatic pathway. Nat Commun. 2014;5:3026.
  • Zhu ZG, Zhang Y-HP. In vitro metabolic engineering of bioelectricity generation by the complete oxidation of glucose. Metab Eng. 2017;39:110–116.
  • Wu R, Ma C, Zhang Y-HP, et al. Complete oxidation of xylose for bioelectricity generation by reconstructing a bacterial xylose utilization pathway in vitro. ChemCatChem. 2018;10(9):2030–2035.
  • Zhang Y-HP, Zhu Z. 2018. Complete oxidation of sugars to electricity by using cell-free synthetic enzymatic pathways. US Patent 10,128,522.
  • Allain EJ. Cell-free ethanol production: the future of fuel ethanol? J Chem Technol Biotechnol. 2007;82(2):117–120.
  • Ye X, Honda K, Sakai T, et al. Synthetic metabolic engineering-a novel, simple technology for designing a chimeric metabolic pathway. Microb Cell Fact. 2012;11(1):120.
  • Opgenorth PH, Korman TP, Iancu L, et al. A molecular rheostat maintains ATP levels to drive a synthetic biochemistry system. Nat Chem Biol. 2017;13(9):938–942.
  • Shi T, Liu S, Zhang Y-HPJ. CO2 fixation for malate synthesis energized by starch via in vitro metabolic engineering. Metab Eng. 2019;55:152–160.
  • Litsanov B, Brocker M, Bott M. Toward homosuccinate fermentation: metabolic engineering of Corynebacterium glutamicum for anaerobic production of succinate from glucose and formate. Appl Environ Microbiol. 2012;78(9):3325–3337.
  • Kawai S, Mori S, Mukai T, et al. Inorganic polyphosphate/ATP-NAD kinase of Micrococcus flavus and Mycobacterium tuberculosis H37Rv. Biochem Biophys Res Commun. 2000;276(1):57–63.
  • Lindner SN, Niederholtmeyer H, Schmitz K, et al. Polyphosphate/ATP-dependent NAD kinase of Corynebacterium glutamicum: biochemical properties and impact of ppnK overexpression on lysine production. Appl Microbiol Biotechnol. 2010;87(2):583–593.
  • Sakuraba H, Kawakami R, Ohshima T. First archaeal inorganic polyphosphate/ATP-dependent NAD kinase, from hyperthermophilic Archaeon Pyrococcus horikoshii: cloning, expression, and characterization. Appl Environ Microbiol. 2005;71(8):4352–4358.
  • Kawai S, Mori S, Mukai T, et al. Establishment of a mass-production system for NADP using bacterial inorganic polyphosphate/ATP-NAD kinase. J Biosci Bioeng. 2001;92(5):447–452.
  • Nagata R, Fujihashi M, Sato T, et al. Identification of a pyrophosphate-dependent kinase and its donor selectivity determinants. Nat Commun. 2018;9(1):1765.
  • Nakamichi Y, Yoshioka A, Kawai S, et al. Conferring the ability to utilize inorganic polyphosphate on ATP-specific NAD kinase. Sci Rep. 2013;3:2632.
  • Saito K, Ohtomo R, Kuga-Uetake Y, et al. Direct labeling of polyphosphate at the ultrastructural level in Saccharomyces cerevisiae by using the affinity of the polyphosphate binding domain of Escherichia coli exopolyphosphatase. Appl Environ Microbiol. 2005;71(10):5692–5701.
  • Cao H, Nie K, Li C, et al. Rational design of substrate binding pockets in polyphosphate kinase for use in cost-effective ATP-dependent cascade reactions. Appl Microbiol Biotechnol. 2017;101(13):5325–5332.
  • Goldenzweig A, Fleishman SJ. Principles of protein stability and their application in computational design. Annu Rev Biochem. 2018;87(1):105–129.
  • Liu Q, Xun G, Feng Y. The state-of-the-art strategies of protein engineering for enzyme stabilization. Biotechnol Adv. 2019;37(4):530–537.
  • Yu H, Huang H. Engineering proteins for thermostability through rigidifying flexible sites. Biotechnol Adv. 2014;32(2):308–315.
  • Bernal C, Rodríguez K, Martínez R. Integrating enzyme immobilization and protein engineering: an alternative path for the development of novel and improved industrial biocatalysts. Biotechnol Adv. 2018;36(5):1470–1480.
  • Kazenwadel F, Franzreb M, Rapp BE. Synthetic enzyme supercomplexes: co-immobilization of enzyme cascades. Anal Methods. 2015;7(10):4030–4037.
  • Sheldon RA, van Pelt S. Enzyme immobilisation in biocatalysis: why, what and how. Chem Soc Rev. 2013;42(15):6223–6235.
  • Liese A, Hilterhaus L. Evaluation of immobilized enzymes for industrial applications. Chem Soc Rev. 2013;42(15):6236–6249.
  • Schoevaart R, Wolbers MW, Golubovic M, et al. Preparation, optimization, and structures of cross-linked enzyme aggregates (CLEAs). Biotechnol Bioeng. 2004;87(6):754–762.
  • Sheldon R. Cross-linked enzyme aggregates (CLEAs): stable and recyclable biocatalysts. Biochem Soc Trans. 2007;35(Pt 6):1583–1587.
  • Dalal S, Kapoor M, Gupta MN. Preparation and characterization of combi-CLEAs catalyzing multiple non-cascade reactions. J Mol Catal B-Enzymatic. 2007;44(3–4):128–132.
  • Scism RA, Bachmann BO. Five-component cascade synthesis of nucleotide analogues in an engineered self-immobilized enzyme aggregate. Chembiochem. 2010;11(1):67–70.
  • Xu M-Q, Li F-L, Yu W-Q, et al. Combined cross-linked enzyme aggregates of glycerol dehydrogenase and NADH oxidase for high efficiency in situ NAD+ regeneration. Int J Biol Macromol. 2020;144:1013–1021.
  • Betancor L, Berne C, Luckarift HR, et al. Coimmobilization of a redox enzyme and a cofactor regeneration system. Chem Commun. 2006;(34):3640–3642.
  • van Dongen S, Nallani M, Cornelissen J, et al. A three-enzyme cascade reaction through positional assembly of enzymes in a polymersome nanoreactor. Chemistry. 2009;15(5):1107–1114.,
  • Wilner OI, Weizmann Y, Gill R, et al. Enzyme cascades activated on topologically programmed DNA scaffolds. Nat Nanotechnol. 2009;4(4):249–254.
  • Mansson MO, Siegbahn N, Mosbach K. Site-to-site directed immobilization of enzymes with bis-NAD analogues. Proc Natl Acad Sci USA. 1983;80(6):1487–1491.
  • Hülsewede D, Meyer L-E, von Langermann J. Application of in situ product crystallization and related techniques in biocatalytic processes. Chemistry. 2019;25(19):4871–4884.
  • Lye GJ, Woodley JM. Application of in situ product-removal techniques to biocatalytic processes. Trends Biotechnol. 1999;17(10):395–402.
  • Woodley JM, Bisschops M, Straathof AJJ, et al. Future directions for in-situ product removal (ISPR). J Chem Technol Biotechnol. 2008;83(2):121–123.

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