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Review Article

Strategies and perspectives of assembling multi-enzyme systems

, , , , &
Pages 1024-1037 | Received 21 Apr 2016, Accepted 12 Dec 2016, Published online: 20 Apr 2017

References

  • Reynolds KA. Combinatorial biosynthesis: lesson learned from nature. Proc Natl Acad Sci USA. 1998;95:12744–12746.
  • Wu F, Minteer S. Krebs cycle metabolon: structural evidence of substrate channeling revealed by cross-linking and mass spectrometry. Angew Chem Int Ed Engl. 2015;54:1851–1854.
  • Conrado RJ, Varner JD, DeLisa MP. Engineering the spatial organization of metabolic enzymes: mimicking nature's synergy. Curr Opin Biotechnol. 2008;19:492–499.
  • Hezaveh S, Zeng AP, Jandt U. Human pyruvate dehydrogenase complex E2 and E3BP core subunits: new models and insights from molecular dynamics simulations. J Phys Chem B. 2016;120:4399–4409.
  • Liu Y, Du J, Yan M, et al. Biomimetic enzyme nanocomplexes and their use as antidotes and preventive measures for alcohol intoxication. Nat Nanotechnol. 2013a;8:187–192.
  • Marsh JA, Teichmann SA. Structure, dynamics, assembly, and evolution of protein complexes. Annu Rev Biochem. 2015;84:551–575.
  • Channon K, Bromley EH, Woolfson DN. Synthetic biology through biomolecular design and engineering. Curr Opin Struct Biol. 2008;18:491–498.
  • Fang BS, Chen HW. Process for preparing 1,3-propylene glycol and dihydroxy acetone by biocatalytic conversion of glycerol, China patent CN1840668A; 2006.
  • France SP, Hussain S, Hill AM, et al. One Pot Cascade synthesis of mono-and di-substituted piperidines and pyrrolidines using carboxylic acid reductase (CAR), ω-transaminase (ω-TA) and imine reductase (IRED) biocatalysts. ACS Catal. 2016;6:3753–3759.
  • Matosevic S, Lye GJ, Baganz F. Immobilised enzyme microreactor for screening of multi-step bioconversions: characterisation of a de novo transketolase-omega-transaminase pathway to synthesise chiral amino alcohols. J Biotechnol. 2011;155:320–329.
  • Ni Y, Xu JH. Biocatalytic ketone reduction: a green and efficient access to enantiopure alcohols. Biotechnol Adv. 2012;30:1279–1288.
  • Ardao I, Hwang ET, Zeng AP. In vitro multienzymatic reaction systems for biosynthesis. Adv Biochem Eng Biotechnol. 2013;137:153–184.
  • Cui JD, Jia SR. Optimization protocols and improved strategies of cross-linked enzyme aggregates technology: current development and future challenges. Crit Rev Biotechnol. 2015;35:15–28.
  • Schoffelen S, van Hest JCM. Multi-enzyme systems: bringing enzymes together in vitro. Soft Matter. 2012;8:1736–1746.
  • Wang P. Nanoscale engineering for smart biocatalysts with fine-tuned properties and functionalitiesed. Top Catal. 2012;55:1107–1113.
  • Zhang Y-HP. Substrate channeling and enzyme complexes for biotechnological applications. Biotechnol Adv. 2011;29:715–725.
  • Xue R, Woodley JM. Process technology for multi-enzymatic reaction systems. Bioresour Technol. 2012;115:183–195.
  • Muschiol J, Peters C, Oberleitner N, et al. Cascade catalysis-strategies and challenges en route to preparative synthetic biology. Chem Commun (Camb). 2015;51:5798–5811.
  • Oroz-Guinea I, García-Junceda E. Enzyme catalysed tandem reactions. Curr Opin Chem Biol. 2013;17:236–249.
  • Hwang ET, Gu MB. Enzyme stabilization by nano/microsized hybrid materials. Eng Life Sci. 2013;13:49–61.
  • Jia F, Narasimhan B, Mallapragada S. Materials-based strategies for multi-enzyme immobilization and co-localization: a review. Biotechnol Bioeng. 2014;111:209–222.
  • Ke YG, Ong LL, Shih WM, et al. Three-dimensional structures self-assembled from DNA bricks. Science. 2012;338:1177–1183.
  • Wilner OI, Weizmann Y, Gill R, et al. Enzyme cascades activated on topologically programmed DNA scaffolds. Nat Nanotechnol. 2009;4:249–254.
  • Simmel FC. DNA-based assembly lines and nanofactories. Curr Opin Biotechnol. 2012;23:516–521.
  • Nojima T, Konno H, Kodera N, et al. Nano-scale alignment of proteins on a flexible DNA backbone. PLoS One. 2012;7:e52534.
  • Niemeyer CM, Koehler J, Wuerdemann C. DNA-directed assembly of bienzymic complexes from in vivo biotinylated NAD(P)H:FMN oxidoreductase and luciferase. Chembiochem. 2002;3:242–245.
  • Erkelenz M, Kuo CH, Niemeyer CM. DNA-mediated assembly of cytochrome P450 BM3 subdomains. J Am Chem Soc. 2011;133:16111–16118.
  • Chi-Hsien K, Niemeyer CM, Fruk L. Bimetallic Copper-heme-protein-DNA hybrid catalyst for diels alder reaction. Croat Chem Acta. 2011;84:269–275.
  • Fu J, Yang YR, Johnson-Buck A, et al. Multi-enzyme complexes on DNA scaffolds capable of substrate channelling with an artificial swinging arm. Nat Nanotechnol. 2014;9:531–536.
  • Müller J, Niemeyer CM. DNA-directed assembly of artificial multienzyme complexes. Biochem Biophys Res Commun. 2008;377:62–67.
  • Shimada J, Maruyama T, Kitaoka M, et al. Programmable protein-protein conjugation via DNA-based self-assembly. Chem Commun (Camb). 2012;48:6226–6228.
  • Delebecque CJ, Lindner AB, Silver PA, et al. Organization of intracellular reactions with rationally designed RNA assemblies. Science. 2011;333:470–474.
  • Van Nguyen K, Giroud F, Minteer SD. Improved bioelectrocatalytic oxidation of sucrose in a biofuel cell with an enzyme cascade sssembled on a DNA scaffold. J Electrochem Soc. 2014;161:H930–H9H3.
  • Xin L, Zhou C, Yang Z, et al. Regulation of an enzyme cascade reaction by a DNA machine. Small. 2013;9:3088–3091.
  • Piperberg G, Wilner OI, Yehezkeli O, et al. Control of bioelectrocatalytic transformations on DNA scaffolds. J Am Chem Soc. 2009;131:8724–8725.
  • Charles IG, Keyte JW, Brammar WJ, et al. The isolation and nucleotide sequence of the complex AROM locus of Aspergillus nidulans. Nucleic Acids Res. 1986;14:2201–2213.
  • Haga T, Hirakawa H, Nagamune T. Fine tuning of spatial arrangement of enzymes in a PCNA-mediated multienzyme complex using a rigid poly-L-proline linker. PLoS One. 2013;8:e75114.
  • Huang Z, Ye F, Zhang C, et al. Rational design of a tripartite fusion protein of heparinase I enables one-step affinity purification and real-time activity detection. J Biotechnol. 2013;163:30–37.
  • Iturrate L, Sanchez-Moreno I, Doyaguez EG, et al. Substrate channelling in an engineered bifunctional aldolase/kinase enzyme confers catalytic advantage for C–C bond formation. Chem Commun. 2009;13:1721–1723.
  • Yourno J, Kohno T, Roth JR. Enzyme evolution: generation of a bifunctional enzyme by fusion of adjacent genes. Nature. 1970;228:820–824.
  • Fang BS, Jiang W, Zhou Q, et al. Codon-optimized NADH oxidase gene expression and gene fusion with glycerol dehydrogenase for bienzyme system with cofactor regeneration. PLoS One. 2015;10:e0128412.
  • Hong SY, Lee JS, Cho KM, et al. Assembling a novel bifunctional cellulase-xylanase from Thermotoga maritima by end-to-end fusion. Biotechnol Lett. 2006;28:1857–1862.
  • Elleuche S. Bringing functions together with fusion enzymes-from nature's inventions to biotechnological applications. Appl Microbiol Biotechnol. 2015;99:1545–1556.
  • Chichili VPR, Kumar V, Sivaraman J. Linkers in the structural biology of protein–protein interactions. Protein Sci. 2013;22:153–167.
  • Choi KY, Jung E, Yun H, et al. Engineering class I cytochrome P450 by gene fusion with NADPH-dependent reductase and S. avermitilis host development for daidzein biotransformation. Appl Microbiol Biotechnol. 2014;98:8191–8200.
  • Lu LL, Yang YY, Lin H, et al. Construction, expression and characterization of fusion enzyme containing azoreductase and glucose 1-dehydrogenase for dye removal. Int Biodeter Biodegr. 2014;87:81–86.
  • Ellis RJ, Minton AP. Cell biology: join the crowd. Nature. 2003;425:27–28.
  • Baneyx F, Mujacic M. Recombinant protein folding and misfolding in Escherichia coli. Nat Biotechnol. 2004;22:1399–1408.
  • Heck T, Faccio G, Richter M, et al. Enzyme-catalyzed protein crosslinking. Appl Microbiol Biotechnol. 2013;97:461–475.
  • Chen X, Zaro JL, Shen WC. Fusion protein linkers: property, design and functionality. Adv Drug Deliv Rev. 2013;65:1357–1369.
  • Rizk M, Antranikian G, Elleuche S. End-to-end gene fusions and their impact on the production of multifunctional biomass degrading enzymes. Biochem Biophys Res Commun. 2012;428:1–5.
  • Lamed R, Setter E, Bayer EA. Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum. J Bacteriol. 1983;156:828–836.
  • Bayer EA, Belaich JP, Shoham Y, et al. The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol. 2004;58:521–554.
  • Bayer EA, Morag E, Lamed R. The cellulosome-a treasure-trove for biotechnology. Trends Biotechnol. 1994;12:379–386.
  • Moraïs S, Morag E, Barak Y, et al. Deconstruction of lignocellulose into soluble sugars by native and designer cellulosomes. MBio. 2012;3:1–10.
  • Liu F, Banta S, Chen W. Functional assembly of a multi-enzyme methanol oxidation cascade on a surface-displayed trifunctional scaffold for enhanced NADH production. Chem Commun. 2013b;49:3766–3768.
  • Barak Y, Handelsman T, Nakar D, et al. Matching fusion protein systems for affinity analysis of two interacting families of proteins: the cohesin-dockerin interaction. J Mol Recognit. 2005;18:491–501.
  • Jindou S, Kajino T, Inagaki M, et al. Interaction between a type-II dockerin domain and a type-II cohesin domain from Clostridium thermocellum cellulosome. Biosci Biotechnol Biochem. 2004;68:924–926.
  • Chiang CJ, Lin LJ, Wang ZW, et al. Design of a noncovalently linked bifunctional enzyme for whole-cell biotransformation. Process Biochem. 2014;49:1122–1128.
  • You C, Myung S, Zhang Y-HP. Facilitated substrate channeling in a self-assembled trifunctional enzyme complex. Angew Chem Int Ed Engl. 2012;51:8787–8790.
  • Tsai SL, Oh J, Singh S, et al. Functional assembly of minicellulosomes on the Saccharomyces cerevisiae cell surface for cellulose hydrolysis and ethanol production. Appl Environ Microbiol. 2009;75:6087–6093.
  • Tsai SL, DaSilva NA, Chen W. Functional display of complex cellulosomes on the yeast surface via adaptive assembly. ACS Synth Biol. 2013;2:14–21.
  • Caspi J, Barak Y, Haimovitz R, et al. Effect of linker length and dockerin position on conversion of a Thermobifida fusca endoglucanase to the cellulosomal mode. Appl Environ Microbiol. 2009;75:7335–7342.
  • Perret S, Bélaich A, Fierobe HP, et al. Towards designer cellulosomes in Clostridia: mannanase enrichment of the cellulosomes produced by Clostridium cellulolyticum. J Bacteriol. 2004;186:6544–6552.
  • Jeon SD, Lee JE, Kim SJ, et al. Analysis of selective, high protein–protein binding interaction of cohesin-dockerin complex using biosensing methods . Biosens Bioelectron. 2012;35:382–389.
  • You C, Zhang Y-HP. Self-assembly of synthetic metabolons through synthetic protein scaffolds: one-step purification, co-immobilization, and substrate channeling. ACS Synth Biol. 2013;2:102–110.
  • Vazana Y, Barak Y, Unger T, et al. A synthetic biology approach for evaluating the functional contribution of designer cellulosome components to deconstruction of cellulosic substrates. Biotechnol Biofuels. 2013;6:182.
  • Lee H, DeLoache WC, Dueber JE. Spatial organization of enzymes for metabolic engineering. Metab Eng. 2012;14:242–251.
  • Chen AH, Silver PA. Designing biological compartmentalization. Trends Cell Biol. 2012;22:662–670.
  • Tamura A, Fukutani Y, Takami T, et al. Packaging guest proteins into the encapsulin nanocompartment from Rhodococcus erythropolis N771. Biotechnol Bioeng. 2015;112:13–20.
  • Sasaki E, Hilvert D. Self-assembly of proteinaceous multishell structures mediated by a supercharged protein. J Phys Chem B. 2016;120:6089–6095.
  • Wörsdörfer B, Woycechowsky KJ, Hilvert D. Directed evolution of a protein container. Science. 2011;331:589–592.
  • Chessher A, Breitling R, Takano E. Bacterial microcompartments: biomaterials for synthetic biology-based compartmentalization strategies. ACS Biomater Sci Eng. 2015;1:345–351.
  • Ferrer-Miralles N, Rodríguez-Carmona E, Corchero JL, et al. Engineering protein self-assembling in protein-based nanomedicines for drug delivery and gene therapy. Crit Rev Biotechnol. 2015;35:209–221.
  • Polka JK, Hays SG, Silver PA. Building spatial synthetic biology with compartments, scaffolds, and communities. Cold Spring Harb Perspect Biol. 2016;8:a024018.
  • Fegan A, Kumarapperuma SC, Wagner CR. Chemically self-assembled antibody nanostructures as potential drug carriers. Mol Pharm. 2012;9:3218–3227.
  • Li Q, So CR, Fegan A, et al. Chemically self-assembled antibody nanorings (CSANs): design and characterization of an anti-CD3 IgM biomimetic. J Am Chem Soc. 2010;132:17247–17257.
  • Chou TF, So C, White BR, et al. Enzyme nanorings. ACS Nano. 2008;2:2519–2525.
  • Carlson JC, Jena SS, Flenniken M, et al. Chemically controlled self-assembly of protein nanorings. J Am Chem Soc. 2006;128:7630–7638.
  • Bai Y, Luo Q, Liu J. Protein self-assembly via supramolecular strategies. Chem Soc Rev. 2016;45:2756–2767.
  • Zorn JA, Wells JA. Turning enzymes ON with small molecules. Nat Chem Biol. 2010;6:179–188.
  • Liao YP, Chen S, Wang DL, et al. Structure of formaldehyde dehydrogenase from Pseudomonas aeruginosa: the binary complex with the cofactor NAD+. Acta Crystallogr F Struct Biol Cryst Commun. 2013;69:967–972.
  • Sanli G, Blaber M. Structural assembly of the active site in an aldo-keto reductase by NADPH cofactor. J Mol Biol. 2001;309:1209–1218.
  • Tahallah N, van den Heuvel RH, van den Berg WA, et al. Cofactor-dependent assembly of the flavoenzyme vanillyl-alcohol oxidase. J Biol Chem. 2002;277:36425–36432.
  • Tang H, Rothery RA, Weiner JH. A variant conferring cofactor-dependent assembly of Escherichia coli dimethylsulfoxide reductase. Biochim Biophys Acta. 2013;1827:730–737.
  • Fang BS, Zhong HP. 2011. Method for carrying out coupling immobilization on coenzyme and coenzyme dependent enzyme. Chinese Patent 201110068888.9.
  • Månsson M, Siegbahn N, Mosbach K. Site-to-site directed immobilization of enzymes with bis-NAD analogues. Proc Natl Acad Sci USA. 1983;80:1487–1491.
  • Oohora K, Onoda A, Hayashi T. Supramolecular assembling systems formed by heme-heme pocket interactions in hemoproteins. Chem Commun (Camb). 2012;48:11714–11726.
  • Fang BS, Niu J, Ren H, et al. Mechanistic study of manganese-substituted glycerol dehydrogenase using a kinetic and thermodynamic analysis. PLoS One. 2014;9:e99162.
  • Wang SZ, Wang J, Zhou XF, et al. The improvement of stability, activity, and substrate promiscuity of glycerol dehydrogenase substituted by divalent metal ions. Biotechnol Bioproc E. 2013;18:796–800.
  • Bogdan ND, Matache M, Meier VM, et al. Protein-inorganic array construction: design and synthesis of the building blocks. Chemistry. 2010;16:2170–2180.
  • Huard DJ, Kane KM, Tezcan FA. Re-engineering protein interfaces yields copper-inducible ferritin cage assembly. Nat Chem Biol. 2013;9:169–176.
  • Thomson AJ, Gray HB. Bio-inorganic chemistry. Curr Opin Chem Biol. 1998;2:155–158.
  • Ueno T. Porous protein crystals as reaction vessels. Chemistry. 2013;19:9096–9102.
  • Zhang YH, Ren H, Wang YL, et al. Bioinspired immobilization of glycerol dehydrogenase by metal ion-chelated polyethyleneimines as artificial polypeptides. Sci Rep. 2016;6:24163.
  • Salgado EN, Ambroggio XI, Brodin JD, et al. Metal templated design of protein interfaces. Proc Natl Acad Sci USA. 2010;107:1827–1832.
  • Zhang W, Luo Q, Miao L, et al. Self-assembly of glutathione S-transferase into nanowires. Nanoscale. 2012;4:5847–5851.
  • Hou C, Li J, Zhao L, et al. Construction of protein nanowires through cucurbit[8]uril-based highly specific host-guest interactions: an approach to the assembly of functional proteins. Angew Chem Int Ed Engl. 2013;52:5590–5593.
  • Bai Y, Luo Q, Zhang W, et al. Highly ordered protein nanorings designed by accurate control of glutathione S-transferase self-assembly. J Am Chem Soc. 2013;135:10966–10969.
  • Grove A, Kushwaha AK, Nguyen KH. 2015. Determining the role of metal binding in protein cage assembly. In: Orner PB, editor. Protein cages: methods and protocols. New York (NY): Springer New York. p. 91–100.
  • Salgado EN, Radford RJ, Tezcan FA. Metal-directed protein self-assembly. Acc Chem Res. 2010;43:661–672.
  • Bogdan ND, Matache M, Roiban G-D, et al. Metal ion mediated self-assembly directed formation of protein arrays. Biomacromolecules. 2011;12:3400–3405.
  • Brodin JD, Carr JR, Sontz PA, et al. Exceptionally stable, redox-active supramolecular protein assemblies with emergent properties. Proc Natl Acad Sci USA. 2014;111:2897–2902.
  • Sanghamitra NJ, Ueno T. Expanding coordination chemistry from protein to protein assembly. Chem Commun (Camb). 2013;49:4114–4126.
  • Sontz PA, Song WJ, Tezcan FA. Interfacial metal coordination in engineered protein and peptide assemblies. Curr Opin Chem Biol. 2014;19:42–49.
  • Linko V, Nummelin S, Aarnos L, et al. DNA-based enzyme reactors and systems. Nanomaterials. 2016;6:139.
  • Wang SZ, Fang BS, Zhang YH, et al. Coordination immobilization of multi-enzyme by metal ions chelated polyethyleneimine, China patent CN105063010A; 2015a.
  • Whitelam S, Jack RL. The statistical mechanics of dynamic pathways to self-assembly. Annu Rev Phys Chem. 2015;66:143–163.
  • Liese A, Hilterhaus L. Evaluation of immobilized enzymes for industrial applications. Chem Soc Rev. 2013;42:6236–6249.
  • Bale JB, Gonen S, Liu Y, et al. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science. 2016;353:389–394.
  • King NP, Bale JB, Sheffler W, et al. Accurate design of co-assembling multi-component protein nanomaterials. Nature. 2014;510:103–108.
  • Kabiri M, Unsworth LD. Application of isothermal titration calorimetry for characterizing thermodynamic parameters of biomolecular interactions: peptide self-assembly and protein adsorption case studies. Biomacromolecules. 2014;15:3463–3473.
  • Averick S, Karacsony O, Mohin J, et al. Cooperative, reversible self-assembly of covalently pre-linked proteins into giant fibrous structures. Angew Chem Int Ed Engl. 2014;53:8050–8055.
  • Schreck JS, Yuan JM. A statistical mechanical approach to protein aggregation. J Chem Phys. 2011;135:235102
  • Schreck JS, Yuan JM. A kinetic study of amyloid formation: fibril growth and length distributions. J Phys Chem B. 2013;117:6574–6583.
  • McManus JJ, Charbonneau P, Zaccarelli E, et al. The physics of protein self-assembly. Curr Opin Colloid Interface Sci. 2016;22:73–79.
  • Alber F, Forster F, Korkin D, et al. Integrating diverse data for structure determination of macromolecular assemblies. Annu Rev Biochem. 2008;77:443–477.
  • Patel MS, Nemeria NS, Furey W, et al. The pyruvate dehydrogenase complexes: structure-based function and regulation. J Biol Chem. 2014;289:16615–16623.
  • Doerr A. Single-particle electron cryomicroscopy. Nat Methods. 2014;11:30.
  • DiMaio F, Echols N, Headd JJ, et al. Improved low-resolution crystallographic refinement with Phenix and Rosetta. Nat Methods. 2013;10:1102–1104.
  • Bunkóczi G, McCoy AJ, Echols N, et al. Macromolecular X-ray structure determination using weak, single-wavelength anomalous data. Nat Methods. 2014;12:127–130.
  • Różycki B, Boura E. Large, dynamic, multi-protein complexes: a challenge for structural biology. J Phys Condens Matter. 2014;26:463103.
  • Miles EW, Rhee S, Davies DR. The molecular basis of substrate channeling. J Biol Chem. 1999;274:12193–12196.
  • Knighton DR, Kan CC, Howland E, et al. Structure of and kinetic channelling in bifunctional dihydrofolate reductase-thymidylate synthase. Nat Struct Biol. 1994;1:186–194.
  • Idan O, Hess H. Origins of activity enhancement in enzyme cascades on scaffolds. ACS Nano. 2013;7:8658–8665.
  • Stern J, Kahn A, Vazana Y, et al. Significance of relative position of cellulases in designer cellulosomes for optimized cellulolysis. PLoS One. 2015;10:e0127326.
  • Lin JL, Palomec L, Wheeldon I. Design and analysis of enhanced catalysis in scaffolded multienzyme cascade reactions. ACS Catal. 2014;4:505–511.
  • Berka K, Sehnal D, Banà P, et al. Anatomy of enzyme channels. BMC Bioinformatics. 2014;15:379.
  • Jemli S, Ayadi-Zouari D, Hlima HB, et al. Biocatalysts: application and engineering for industrial purposes. Crit Rev Biotechnol. 2016;36:246–258.
  • Jiang W, Wang SZ, Wang YP, et al. Key enzymes catalyzing glycerol to 1,3-propanediol. Biotechnol Biofuels. 2016;9:57.
  • Hold C, Billerbeck S, Panke S. Forward design of a complex enzyme cascade reaction. Nat Commun. 2016;7:12971.

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