Substrate channelling as an approach to cascade reactions

Nature Chemistry

Volumn 8, Issue 4, 2016, Pages 299-309

  Wheeldon, Ian ^a   Minteer, Shelley D ^b   Banta, Scott ^c   Barton, Scott Calabrese ^d   Atanassov, Plamen ^e   Sigman, Matthew ^b  

^a University of California Riverside   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c Columbia University ^*  (United States)

^d Michigan State University   (United States)

^e University of New Mexico   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME;

BIOCATALYSIS; CHEMISTRY; DIFFUSION; ENZYME ACTIVE SITE; METABOLISM;

BIOCATALYSIS; CATALYTIC DOMAIN; DIFFUSION; ENZYMES;

EID: 84961644292     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.2459     Document Type: Review

References (113)

1. Spivey, H. O. & Ovadi, J. Substrate channeling. Methods 19, 306-321 (1999).
2. Miles, E. W., Rhee, S. & Davies, D. R. The molecular basis of substrate channeling. J. Biol. Chem. 274, 12193-12196 (1999).
3. Yamada, Y. et al. Nanocrystal bilayer for tandem catalysis. Nature Chem. 3, 372-376 (2011).
4. Zhao, M. T. et al. Core-shell palladium nanoparticle@metal-organic frameworks as multifunctional catalysts for cascade reactions. J. Am. Chem. Soc. 136, 1738-1741 (2014).
5. Motokura, K. et al. An acidic layered clay is combined with a basic layered clay for one-pot sequential reactions. J. Am. Chem. Soc. 127, 9674-9675 (2005).
6. Yang, Y. et al. A yolk-shell nanoreactor with a basic core and an acidic shell for cascade reactions. Angew. Chem. Int. Ed. 51, 9164-9168 (2012).
7. Li, P. et al. Core-shell structured mesoporous silica as acid-base bifunctional catalyst with designated diffusion path for cascade reaction sequences. Chem. Commun. 48, 10541-10543 (2012).
8. Zhang, Y. H. Substrate channeling and enzyme complexes for biotechnological applications. Biotechnol. Adv. 29, 715-725 (2011).
9. Dueber, J. E. et al. Synthetic protein scaffolds provide modular control over metabolic flux. Nature Biotechnol. 27, 753-759 (2009).
10. Conrado, R. J. et al. DNA-guided assembly of biosynthetic pathways promotes improved catalytic efficiency. Nucleic Acids Res. 40, 1879-1889 (2011).
11. Delebecque, C. J., Lindner, A. B., Silver, P. A. & Aldaye, F. A. Organization of intracellular reactions with rationally designed RNA assemblies. Science 333, 470-474 (2011).
12. Fu, J. L., Liu, M. H., Liu, Y., Woodbury, N. W. & Yan, H. Interenzyme substrate diffusion for an enzyme cascade organized on spatially addressable DNA nanostructures. J. Am. Chem. Soc. 134, 5516-5519 (2012).
13. Wilner, O. I., Shimron, S., Weizmann, Y., Wang, Z. G. & Willner, I. Self-assembly of enzymes on DNA scaffolds: en route to biocatalytic cascades and the synthesis of metallic nanowires. Nano Lett. 9, 2040-2043 (2009).
14. Muller, J. & Niemeyer, C. M. DNA-directed assembly of artificial multienzyme complexes. Biochem. Biophys. Res. Commun. 377, 62-67 (2008).
15. Vriezema, D. M. et al. Positional assembly of enzymes in polymersome nanoreactors for cascade reactions. Angew. Chem. Int. Ed. 46, 7378-7382 (2007).
16. Wang, X. L. et al. Bioinspired approach to multienzyme cascade system construction for efficient carbon dioxide reduction. ACS Catal. 4, 962-972 (2014).
17. Bauler, P., Huber, G., Leyh, T. & McCammon, J. A. Channeling by proximity: the catalytic advantages of active site colocalization using brownian dynamics. J. Phys. Chem. Lett. 1, 1332-1335 (2010).
18. Eun, C., Kekenes-Huskey, P. M., Metzger, V. T. & McCammon, J. A. A model study of sequential enzyme reactions and electrostatic channeling. J. Chem. Phys. 140, 105101 (2014).
19. Knighton, D. R. et al. Structure of and kinetic channeling in bifunctional dihydrofolate reductase-thymidylate synthase. Nature Struct. Biol. 1, 186-194 (1994).
20. Hyde, C. C., Ahmed, S. A., Padlan, E. A., Miles, E. W. & Davies, D. R. Three-dimensional structure of the tryptophan synthase alpha 2 beta 2 multienzyme complex from Salmonella typhimurium. J. Biol. Chem. 263, 17857-17871 (1988).
21. Wang, J. J. et al. Structure and function of the catalytic domain of the dihydrolipoyl acetyltransferase component in Escherichia coli pyruvate dehydrogenase complex. J. Biol. Chem. 289, 15215-15230 (2014).
22. Zhang, C. et al. Autonomic molecular transport by polymer films containing programmed chemical potential gradients. J. Am. Chem. Soc. 137, 5066-5073 (2015).
23. Fu, Y. M. et al. Single-step rapid assembly of DNA origami nanostructures for addressable nanoscale bioreactors. J. Am. Chem. Soc. 135, 696-702 (2013).
24. Yan, J. C. et al. Growth of patterned nanopore arrays of anodic aluminum oxide. Adv. Mater. 15, 2015-2018 (2003).
25. Worsdorfer, B., Woycechowsky, K. J. & Hilvert, D. Directed evolution of a protein container. Science 331, 589-592 (2011).
26. Salles, A. G., Zarra, S., Turner, R. M. & Nitschke, J. R. A self-organizing chemical assembly line. J. Am. Chem. Soc. 135, 19143-19146 (2013).
27. Filice, M. & Palomo, J. M. Cascade reactions catalyzed by bionanostructures. ACS Catal. 4, 1588-1598 (2014).
28. Chng, L. L., Erathodiyil, N. & Ying, J. Y. Nanostructured catalysts for organic transformations. Acc. Chem. Res. 46, 1825-1837 (2013).
29. Margelefsky, E. L., Zeidan, R. K. & Davis, M. E. Cooperative catalysis by silica-supported organic functional groups. Chem. Soc. Rev. 37, 1118-1126 (2008).
30. Kim, E. Y. & Tullman-Ercek, D. Engineering nanoscale protein compartments for synthetic organelles. Curr. Opin. Biotechnol. 24, 627-632 (2013).
31. Schoffelen, S. & van Hest, J. C. M. Chemical approaches for the construction of multi-enzyme reaction systems. Curr. Opin. Struc. Biol. 23, 613-621 (2013).
32. Conrado, R. J., Varner, J. D. & DeLisa, M. P. Engineering the spatial organization of metabolic enzymes: mimicking nature's synergy. Curr. Opin. Biotechnol. 19, 492-499 (2008).
33. Srere, P. A. The metabolon. Trends Biochem. Sci. 10, 109-110 (1985).
34. Srere, P. A. Complexes of sequential metabolic enzymes. Annu. Rev. Biochem. 56, 89-124 (1987).
35. Srere, P. & Mosbach, K. Metabolic compartmentalization: symbiotic, organellar, multienzymatic, and microenvironmental. Annu. Rev. Microbiol. 28, 61-84 (1974).
36. Srere, P. A., Mattiasson, B. & Mosbach, K. An immobilized three-enzyme system: a model for microenvironmental compartemtnation in mitochondria. Proc. Natl Acad. Sci. USA 70, 2534-2538 (1973).
37. Ovádi, J. Physiological significance of metabolic channelling. J. Theor. Biol. 152, 1-22 (1991).
38. Lin, J.-L., Palomec, L. & Wheeldon, I. Design and analysis of enhanced catalysis in scaffolded multienzyme cascade reactions. ACS Catal. 4, 505-511 (2014).
39. Lee, H., DeLoache, W. C. & Dueber, J. E. Spatial organization of enzymes for metabolic engineering. Metab. Eng. 14, 242-251 (2012).
40. Agapakis, C. M., Boyle, P. M. & Silver, P. A. Natural strategies for the spatial optimization of metabolism in synthetic biology. Nature Chem. Biol. 8, 527-535 (2012).
41. Anderson, K. S., Miles, E. W. & Johnson, K. A. Serine modulates substrate channeling in tryptophan synthase - a novel intersubunit triggering mechanism. J. Biol. Chem. 266, 8020-8033 (1991).
42. Dunn, M. F. et al. The tryptophan synthase bienzyme complex transfers indole between the alpha-sites and beta-sites via a 25-30 a long tunnel. Biochemistry 29, 8598-8607 (1990).
43. Carere, J., McKenna, S. E., Kimber, M. S. & Seah, S. Y. K. Characterization of an aldolase-dehydrogenase complex from the cholesterol degradation pathway of Mycobacterium tuberculosis. Biochemistry 52, 3502-3511 (2013).
44. Thoden, J. B., Raushel, F. M., Benning, M. M., Rayment, I. & Holden, H. M. The structure of carbamoyl phosphate synthetase determined to 2.1 angstrom resolution. Acta Crystallogr. D 55, 8-24 (1999).
45. Huang, X. Y. & Raushel, F. M. Restricted passage of reaction intermediates through the ammonia tunnel of carbamoyl phosphate synthetase. J. Biol. Chem. 275, 26233-26240 (2000).
46. Krahn, J. M. et al. Coupled formation of an amidotransferase interdomain ammonia channel and a phosphoribosyltransferase active site. Biochemistry 36, 11061-11068 (1997).
47. Huang, X. Y., Holden, H. M. & Raushel, F. M. Channeling of substrates and intermediates in enzyme-catalyzed reactions. Annu. Rev. Biochem. 70, 149-180 (2001).
48. Raushel, F. M., Thoden, J. B. & Holden, H. M. Enzymes with molecular tunnels. Acc. Chem. Res. 36, 539-548 (2003).
49. Elcock, A. H., Huber, G. A. & McCammon, J. A. Electrostatic channeling of substrates between enzyme active sites: comparison of simulation and experiment. Biochemistry 36, 16049-16058 (1997).
50. Elcock, A. H., Potter, M. J., Matthews, D. A., Knighton, D. R. & McCammon, J. A. Electrostatic channeling in the bifunctional enzyme dihydrofolate reductase-thymidylate synthase. J. Mol. Biol. 262, 370-374 (1996).
51. Lindbladh, C. et al. Preparation and kinetic characterization of a fusion protein of yeast mitochondrial citrate synthase and malate-dehydrogenase. Biochemistry 33, 11692-11698 (1994).
52. Wu, F. & Minteer, S. Krebs cycle metabolon: structural evidence of substrate channeling revealed by cross-linking and mass spectrometry. Angew. Chem. Int. Ed. 54, 1851-1854 (2015).
53. Guynn, R. W., Gelberg, H. J. & Veech, R. L. Equilibrium constants of the malate dehydrogenase, citrate synthase, citrate lyase, and acetyl coenzyme A hydrolysis reactions under physiological conditions. J. Biol. Chem. 248, 6957-6965 (1973).
54. Smolle, M. & Lindsay, J. G. Molecular architecture of the pyruvate dehydrogenase complex: bridging the gap. Biochem. Soc. Trans. 34, 815-818 (2006).
55. Smolle, M. et al. A new level of architectural complexity in the human pyruvate dehydrogenase complex. J. Biol. Chem. 281, 19772-19780 (2006).
56. Zhou, Z. H., McCarthy, D. B., O'Connor, C. M., Reed, L. J. & Stoops, J. K. The remarkable structural and functional organization of the eukaryotic pyruvate dehydrogenase complexes. Proc. Natl Acad. Sci. USA 98, 14802-14807 (2001).
57. Perham, R. N. Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annu. Rev. Biochem. 69, 961-1004 (2000).
58. Leibundgut, M., Maier, T., Jenni, S. & Ban, N. The multienzyme architecture of eukaryotic fatty acid synthases. Curr. Opin. Struc. Biol. 18, 714-725 (2008).
59. Ishikawa, M., Tsuchiya, D., Oyama, T., Tsunaka, Y. & Morikawa, K. Structural basis for channelling mechanism of a fatty acid beta-oxidation multienzyme complex. EMBO J. 23, 2745-2754 (2004).
60. Winkel-Shirley, B. Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol. Plantarum 107, 142-149 (1999).
61. Jorgensen, K. et al. Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant. Biol. 8, 280-291 (2005).
62. Winkel, B. S. Metabolic channeling in plants. Annu. Rev. Plant Biol. 55, 85-107 (2004).
63. Sweetlove, L. J. & Fernie, A. R. The spatial organization of metabolism within the plant cell. Annu. Rev. Plant Biol. 64, 723-746 (2013).
64. Geck, M. K. & Kirsch, J. F. A novel, definitive test for substrate channeling illustrated with the aspartate aminotransferase malate dehydrogenase system. Biochemistry 38, 8032-8037 (1999).
65. Trujillo, M., Donald, R. G. K, Roos, D. S, Greene, P. J. & Santi, D. V. Heterologous expression and characterization of the bifunctional dihydrofolate reductase-thymidylate synthase enzyme of Toxoplasma gondii. Biochemistry 35, 6366-6374 (1996).
66. Sharma, H., Landau, M. J., Vargo, M. A., Spasov, K. A. & Anderson, K. S. First three-dimensional structure of Toxoplasma gondii thymidylate synthase-dihydrofolate reductase: insights for catalysis, interdomain interactions, and substrate channeling. Biochemistry 52, 7305-7317 (2013).
67. Idan, O. & Hess, H. Origins of activity enhancement in enzyme cascades on scaffolds. ACS Nano 7, 8658-8665 (2013).
68. Ljungcrantz, P. et al. Construction of an artificial bifunctional enzyme, beta-galactosidase/galactose dehydrogenase, exhibiting efficient galactose channeling. Biochemistry 28, 8786-8792 (1989).
69. Pettersson, H. & Pettersson, G. Kinetics of the coupled reaction catalysed by a fusion protein of beta-galactosidase and galactose dehydrogenase. Biochim. Biophys. Acta 1549, 155-160 (2001).
70. Climent, M. J., Corma, A., Iborra, S. & Sabater, M. J. Heterogeneous catalysis for tandem reactions. ACS Catal. 4, 870-891 (2014).
71. Kung, H. H. & Kung, M. C. Inspiration from nature for heterogeneous catalysis. Catal. Lett. 144, 1643-1652 (2014).
72. Muschiol, J. Cascade catalysis - strategies and challenges en route to preparative synthetic biology. Chem. Commun. 51, 5798-5811 (2015).
73. Broadwater, S. J., Roth, S. L., Price, K. E., Kobaslija, M. & McQuade, D. T. One-pot multi-step synthesis: a challenge spawning innovation. Org. Biomol. Chem. 3, 2899-2906 (2005).
74. Massong, H., Wang, H. S., Samjeske, G. & Baltruschat, H. The co-catalytic effect of Sn, Ru and Mo decorating steps of Pt(111) vicinal electrode surfaces on the oxidation of CO. Electrochim. Acta 46, 701-707 (2000).
75. Wang, N. & McCammon, J. A. Substrate channeling between the human dihydrofolate reductase and thymidylate synthase. Protein Sci. 25, 79-86 (2016).
76. Lin, J.-L. & Wheeldon, I. Kinetic enhancements in DNA-enzyme nanostructures mimic the sabatier principle. ACS Catal. 3, 560-564 (2013).
77. Gao, Y. et al. Tuning enzyme kinetics through designed intermolecular interactions far from the active site. ACS Catal. 5, 2149-2153 (2015).
78. Murata, H., Cummings, C. S., Koepsel, R. R. & Russell, A. J. Rational tailoring of substrate and inhibitor affinity via ATRP polymer-based protein engineering. Biomacromolecules 15, 2817-2823 (2014).
79. You, C. C., Agasti, S. S., De, M., Knapp, M. J. & Rotello, V. M. Modulation of the catalytic behavior of alpha-chymotrypsin at monolayer-protected nanoparticle surfaces. J. Am. Chem. Soc. 128, 14612-14618 (2006).
80. Fu, J. L. et al. et al. Multi-enzyme complexes on DNA scaffolds capable of substrate channelling with an artificial swinging arm. Nature Nanotech. 9, 531-536 (2014).
81. Wilner, O. I. et al. Enzyme cascades activated on topologically programmed DNA scaffolds. Nature Nanotech. 4, 249-254 (2009).
82. Zhang, F., Jiang, H. Y., Li, X. Y., Wu, X. T. & Li, H. X. Amine-functionalized GO as an active and reusable acid-base bifunctional catalyst for one-pot cascade reactions. ACS Catal. 4, 394-401 (2014).
83. van Dongen, S. F. M., Nallani, M., Cornelissen, J. L. L. M., Nolte, R. J. M. & van Hest, J. C. M. A three-enzyme cascade reaction through positional assembly of enzymes in a polymersome nanoreactor. Chem. Eur. J. 15, 1107-1114 (2009).
84. Huang, X., Li, M. & Mann, S. Membrane-mediated cascade reactions by enzyme-polymer proteinosomes. Chem. Commun. 50, 6278-6280 (2014).
85. Peters, R. J. R. W. et al. Cascade reactions in multicompartmentalized polymersomes. Angew. Chem. Int. Ed. 53, 146-150 (2014).
86. Patterson, D. P., Schwarz, B., Waters, R. S., Gedeon, T. & Douglas, T. Encapsulation of an enzyme cascade within the bacteriophage P22 virus-like particle. ACS Chem. Biol. 9, 359-365 (2014).
87. Park, M., Sun, Q., Liu, F., DeLisa, M. P. & Chen, W. Positional assembly of enzymes on bacterial outer membrane vesicles for cascade reactions. PLoS ONE 9, e97103 (2014).
88. Glasgow, J. E., Asensio, M. A., Jakobson, C. M., Francis, M. B. & Tullman-Ercek, D. Influence of electrostatics on small molecule flux through a protein nanoreactor. ACS Synth. Biol. 4, 1011-1019 (2015).
89. Li, Z. X. et al. Spatial co-localization of multi-enzymes by inorganic nanocrystal-protein complexes. Chem. Commun. 50, 12465-12468 (2014).
90. Buchner, A., Tostevin, F. & Gerland, U. Clustering and optimal arrangement of enzymes in reaction-diffusion systems. Phys. Rev. Lett. 110, 208104 (2013).
91. Alam-Nazki, A. & Krishnan, J. Spatial control of biochemical modification cascades and pathways. Biophys. J. 108, 2912-2924 (2015).
92. Roberts, C. C. & Chang, C.-A. Modeling of enhanced catalysis in multienzyme nanostructures: effect of molecular scaffolds, spatial organization, and concentration. J. Chem. Theory Comput. 11, 286-292 (2015).
93. Freeman, R., Sharon, E., Teller, C. & Willner, I. Control of biocatalytic transformations by programmed DNA assemblies. Chem. Eur. J. 16, 3690-3698 (2010).
94. Xin, L., Zhou, C., Yang, Z. & Liu, D. Regulation of an enzyme cascade reaction by a DNA machine. Small 9, 3088-3091 (2013).
95. Van Nguyen, K., Giroud, F. & Minteer, S. D. Improved bioelectrocatalytic oxidation of sucrose in a biofuel cell with an enzyme cascade assembled on a DNA scaffold. J. Electrochem. Soc. 161, H930-H933 (2014).
96. Moehlenbrock, M. J., Toby, T. K., Waheed, A. & Minteer, S. D. Metabolon catalyzed pyruvate/air biofuel cell. J. Am. Chem. Soc. 132, 6288-6289 (2010).
97. 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. 49, 3766-3768 (2013).
98. Hirakawa, H. & Nagamune, T. Molecular assembly of P450 with ferredoxin and ferredoxin reductase by fusion to PCNA. Chem BioChem 11, 1517-1520 (2010).
99. 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 8, e75114 (2013).
100. Bayer, E. A., Morag, E. & Lamed, R. The cellulosome - a treasure-trove for biotechnology. Trends Biotechnol. 12, 379-386 (1994).
101. You, C., Myung, S. & Zhang, Y. H. P. Facilitated substrate channeling in a self-assembled trifunctional enzyme complex. Angew. Chem. Int. Ed. 51, 8787-8790 (2012).
102. You, C. & Zhang. Y. H. P. Self-assembly of synthetic metabolons through synthetic protein scaffolds: one-step purification, co-immobilization, and substrate channeling. ACS Synth. Biol. 2, 102-110 (2013).
103. You, C. & Zhang, Y. H. P. Annexation of a high-activity enzyme in a synthetic three-enzyme complex greatly decreases the degree of substrate channeling. ACS Synth. Biol. 3, 380-386 (2014).
104. You, C. et al. Enzymatic transformation of nonfood biomass to starch. Proc. Natl Acad. Sci. USA 110, 7182-7187 (2013).
105. Baek, J. M. et al. Butyrate production in engineered Escherichia coli with synthetic scaffolds. Biotechnol. Bioeng. 110, 2790-2794 (2013).
106. Wang, Y. C. & Yu, O. Synthetic scaffolds increased resveratrol biosynthesis in engineered yeast cells. J. Biotechnol. 157, 258-260 (2012).
107. Moon, T. S., Dueber, J. E., Shiue, E. & Prather, K. L. J. Use of modular, synthetic scaffolds for improved production of glucaric acid in engineered E. coli. Metab. Eng. 12, 298-305 (2010).
108. Lee, J. H. et al. Improved production of L-threonine in Escherichia coli by use of a DNA scaffold system. Appl. Environ. Microbiol. 79, 774-782 (2013).
109. Sachdeva, G., Garg, A., Godding, D., Way, J. C. & Silver, P. A. In vivo co-localization of enzymes on RNA scaffolds increases metabolic production in a geometrically dependent manner. Nucleic Acids Res. 42, 9493-9503 (2014).
110. Baillie, G. S. Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. FEBS J. 276, 1790-1799 (2009).
111. McCormick, K. & Baillie, G. S. Compartmentalisation of second messenger signalling pathways. Curr. Opin. Genet. Dev. 27, 20-25 (2014).
112. Castellana, M. et al. Enzyme clustering accelerates processing of intermediates through metabolic channeling. Nature Biotechnol. 32, 1011-1018 (2014).
113. Schneider, T. R. et al. Loop closure and intersubunit communication in tryptophan synthase. Biochemistry 37, 5394-5406 (1998).