A General Tool for Engineering the NAD/NADP Cofactor Preference of Oxidoreductases

ACS Synthetic Biology

Volumn 6, Issue 2, 2017, Pages 326-333

  Cahn, Jackson K B ^a   Werlang, Caroline A ^a   Baumschlager, Armin ^a   Brinkmann Chen, Sabine ^a   Mayo, Stephen L ^b   Arnold, Frances H ^a  

^a California Institute of Technology   (United States)

^b California Institute of Technology   (United States)

Author keywords

cofactor specificity; library design; oxidoreductases; protein engineering; semirational engineering

Indexed keywords

CINNAMYL ALCOHOL DEHYDROGENASE; ENZYME; GLYOXYLATE REDUCTASE; IRON CONTAINING ALCOHOL DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXIDOREDUCTASE; UNCLASSIFIED DRUG; XYLOSE REDUCTASE; ALCOHOL DEHYDROGENASE; ALDEHYDE REDUCTASE;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME ANALYSIS; ENZYME ENGINEERING; ENZYME SPECIFICITY; MICHAELIS MENTEN KINETICS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; GENETICS; PROCEDURES; PROTEIN CONFORMATION; PROTEIN ENGINEERING;

ALCOHOL DEHYDROGENASE; ALCOHOL OXIDOREDUCTASES; ALDEHYDE REDUCTASE; NAD; NADP; OXIDOREDUCTASES; PROTEIN CONFORMATION; PROTEIN ENGINEERING; SUBSTRATE SPECIFICITY;

EID: 85013213122     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.6b00188     Document Type: Article

References (53)

1. Wang, Y., San, K.-Y., and Bennett, G. N. (2013) Cofactor engineering for advancing chemical biotechnology Curr. Opin. Biotechnol. 24, 994-999 10.1016/j.copbio.2013.03.022
2. +-dependent xylitol dehydrogenase increases ethanol production from xylose in recombinant Saccharomyces cerevisiae Appl. Microbiol. Biotechnol. 81, 243-255 10.1007/s00253-008-1649-1
3. Bengtsson, O., Hahn-Hagerdal, B., and Gorwa-Grauslund, M. F. (2009) Xylose reductase from Pichia stipitis with altered coenzyme preference improves ethanolic xylose fermentation by recombinant Saccharomyces cerevisiae Biotechnol. Biofuels 2, 9 10.1186/1754-6834-2-9
4. Hasegawa, S., Uematsu, K., Natsuma, Y., Suda, M., Hiraga, K., Jojima, T., Inui, M., and Yukawa, H. (2012) Improvement of the redox balance increases L-valine production by Corynebacterium glutamicum under oxygen deprivation conditions Appl. Environ. Microbiol. 78, 865-875 10.1128/AEM.07056-11
5. Bastian, S., Liu, X., Meyerowitz, J. T., Snow, C. D., Chen, M. M. Y., and Arnold, F. H. (2011) Engineered ketol-acid reductoisomerase and alcohol dehydrogenase enable anaerobic 2-methylpropan-1-ol production at theoretical yield in Escherichia coli Metab. Eng. 13, 345-352 10.1016/j.ymben.2011.02.004
6. Tamakawa, H., Ikushima, S., and Yoshida, S. (2011) Ethanol production from xylose by a recombinant Candida utilis strain expressing protein-engineered xylose reductase and xylitol dehydrogenase Biosci., Biotechnol., Biochem. 75, 1994-2000 10.1271/bbb.110426
7. Shen, C. R., Lan, E. I., Dekishima, Y., Baez, A., Cho, K. M., and Liao, J. C. (2011) Driving forces enable high-titer anaerobic 1-butanol synthesis in Escherichia coli Appl. Environ. Microbiol. 77, 2905-2915 10.1128/AEM.03034-10
8. + regeneration for production of chiral chemicals PLoS One 5, e8860 10.1371/journal.pone.0008860
9. Scrutton, N. S., Berry, A., and Perham, R. N. (1990) Redesign of the coenzyme specificity of a dehydrogenase by protein engineering Nature 343, 38-43 10.1038/343038a0
10. Khoury, G. A., Fazelinia, H., Chin, J. W., Pantazes, R. J., Cirino, P. C., and Maranas, C. D. (2009) Computational design of Candida boidinii xylose reductase for altered cofactor specificity Protein Sci. 18, 2125-2138 10.1002/pro.227
11. Mesecar, A. D., Stoddard, B. L., and Koshland, D. E., Jr. (1997) Orbital steering in the catalytic power of enzymes: Small structural changes with large catalytic consequences Science 277, 202-206 10.1126/science.277.5323.202
12. Cahn, J. K. B., Baumschlager, A., Brinkmann-Chen, S., and Arnold, F. H. (2016) Mutations in adenine-binding pockets enhance catalytic properties of NAD(P)H-dependent enzymes Protein Eng., Des. Sel. 29, 31-38 10.1093/protein/gzv057
13. Maddock, D. J., Patrick, W. M., and Gerth, M. L. (2015) Substitutions at the cofactor phosphate-binding site of a clostridial alcohol dehydrogenase lead to unexpected changes in substrate specificity Protein Eng., Des. Sel. 28, 251-258 10.1093/protein/gzv028
14. Naylor, C. E., Gover, S., Basak, A. K., Cosgrove, M. S., Levy, H. R., and Adams, M. J. (2001) NADP(+) and NAD(+) binding to the dual coenzyme specific enzyme Leuconostoc mesenteroides glucose 6-phosphate dehydrogenase: Different interdomain hinge angles are seen in different binary and ternary complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 635-648 10.1107/S0907444901003420
15. Kavanagh, K. L., Klimacek, M., Nidetzky, B., and Wilson, D. K. (2003) Structure of xylose reductase bound to NAD(+) and the basis for single and dual co-substrate specificity in family 2 aldo-keto reductases Biochem. J. 373, 319-326 10.1042/bj20030286
16. Campbell, E., Chuang, S., and Banta, S. (2013) Modular exchange of substrate-binding loops alters both substrate and cofactor specificity in a member of the aldo-keto reductase superfamily Protein Eng., Des. Sel. 26, 181-186 10.1093/protein/gzs095
17. Plapp, B. V. (2010) Conformational changes and catalysis by alcohol dehydrogenase Arch. Biochem. Biophys. 493, 3-12 10.1016/j.abb.2009.07.001
18. Brinkmann-Chen, S., Flock, T., Cahn, J. K. B., Snow, C. D., Brustad, E. M., McIntosh, J. A., Meinhold, P., Zhang, L., and Arnold, F. H. (2013) General approach to reversing ketol-acid reductoisomerase cofactor dependence from NADPH to NADH Proc. Natl. Acad. Sci. U. S. A. 110, 10946-10951 10.1073/pnas.1306073110
19. Cahn, J. K. B., Brinkmann-Chen, S., Spatzal, T., Wiig, J. A., Buller, A. R., Einsle, O., Hu, Y., Ribbe, M. W., and Arnold, F. H. (2015) Cofactor specificity motifs and the induced fit mechanism in class I ketol-acid reductoisomerases Biochem. J. 468, 475-484 10.1042/BJ20150183
20. Carugo, O. and Argos, P. (1997) NADP-dependent enzymes. I: Conserved stereochemistry of cofactor binding Proteins: Struct., Funct., Genet. 28, 10-28 10.1002/(SICI)1097-0134(199705)28:1<10::AID-PROT2>3.0.CO;2-N
21. Moodie, S. L., Mitchell, J. B., and Thornton, J. M. (1996) Protein recognition of adenylate: An example of a fuzzy recognition template J. Mol. Biol. 263, 486-500 10.1006/jmbi.1996.0591
22. Denessiouk, K. A., Rantanen, V. V., and Johnson, M. S. (2001) Adenine recognition: a motif present in ATP-, CoA-, NAD-, NADP-, and FAD-dependent proteins Proteins: Struct., Funct., Genet. 44, 282-291 10.1002/prot.1093
23. Wallen, J. R., Paige, C., Mallett, T. C., Karplus, P. A., and Claiborne, A. (2008) Pyridine nucleotide complexes with Bacillus anthracis coenzyme A-disulfide reductase: A structural analysis of dual NAD(P)H specificity Biochemistry 47, 5182-5193 10.1021/bi8002204
24. Brinkmann-Chen, S., Cahn, J. K. B., and Arnold, F. H. (2014) Uncovering rare NADH-preferring ketol-acid reductoisomerases Metab. Eng. 26, 17-22 10.1016/j.ymben.2014.08.003
25. Di Luccio, E., Elling, R. A., and Wilson, D. K. (2006) Identification of a novel NADH-specific aldo-keto reductase using sequence and structural homologies Biochem. J. 400, 105-114 10.1042/BJ20060660
26. Hatrongjit, R. and Packdibamrung, K. (2010) A novel NADP(+)-dependent formate dehydrogenase from Burkholderia stabilis 15516: Screening, purification and characterization Enzyme Microb. Technol. 46, 557-561 10.1016/j.enzmictec.2010.03.002
27. Jensen, C. N., Ali, S. T., Allen, M. J., and Grogan, G. (2014) Exploring nicotinamide cofactor promiscuity in NAD(P)H-dependent flavin containing monooxygenases (FMOs) using natural variation within the phosphate binding loop. Structure and activity of FMOs from Cellvibrio sp. BR and Pseudomonas stutzeri NF13 J. Mol. Catal. B: Enzym. 109, 191-198 10.1016/j.molcatb.2014.08.019
28. Rodriguez-Arnedo, A., Camacho, M., Llorca, F., and Bonete, M. J. (2005) Complete reversal of coenzyme specificity of isocitrate dehydrogenase from Haloferax volcanii Protein J. 24, 259-266 10.1007/s10930-005-6746-8
29. Rosell, A., Valencia, E., Ochoa, W. F., Fita, I., Pares, X., and Farres, J. (2003) Complete reversal of coenzyme specificity by concerted mutation of three consecutive residues in alcohol dehydrogenase J. Biol. Chem. 278, 40573-40580 10.1074/jbc.M307384200
30. Reetz, M. T. and Wu, S. (2008) Greatly reduced amino acid alphabets in directed evolution: Making the right choice for saturation mutagenesis at homologous enzyme positions Chem. Commun. 5499-5501 10.1039/b813388c
31. Mena, M. A. and Daugherty, P. S. (2005) Automated design of degenerate codon libraries Protein Eng., Des. Sel. 18, 559-561 10.1093/protein/gzi061
32. Engqvist, M. K. M. and Nielsen, J. (2015) ANT: Software for generating and evaluating degenerate codons for natural and expanded genetic codes ACS Synth. Biol. 4, 935-938 10.1021/acssynbio.5b00018
33. Cornish-Bowden, A. (1985) Nomenclature for incompletely specified bases in nucleic acid sequences: Reccomendations 1984 Nucleic Acids Res. 13, 3021-3030 10.1093/nar/13.9.3021
34. Fasan, R., Meharenna, Y. T., Snow, C. D., Poulos, T. L., and Arnold, F. H. (2008) Evolutionary history of a specialized P450 propane monooxygenase J. Mol. Biol. 383, 1069-1080 10.1016/j.jmb.2008.06.060
35. Bloom, J. D., Arnold, F. H., and Wilke, C. O. (2007) Breaking proteins with mutations: Threads and thresholds in evolution Mol. Syst. Biol. 3, 76 10.1038/msb4100119
36. Woodyer, R., van der Donk, W. A., and Zhao, H. M. (2003) Relaxing the nicotinamide cofactor specificity of phosphite dehydrogenase by rational design Biochemistry 42, 11604-11614 10.1021/bi035018b
37. Verho, R., Londesborough, J., Penttila, M., and Richard, P. (2003) Engineering redox cofactor regeneration for improved pentose fermentation in Saccharomyces cerevisiae Appl. Environ. Microbiol. 69, 5892-5897 10.1128/AEM.69.10.5892-5897.2003
38. Huffer, S., Roche, C. M., Blanch, H. W., and Clark, D. S. (2012) Escherichia coli for biofuel production: Bridging the gap from promise to practice Trends Biotechnol. 30, 538-545 10.1016/j.tibtech.2012.07.002
39. Rossmann, M. G., Moras, D., and Olsen, K. W. (1974) Chemical and biological evolution of nucleotide-binding protein Nature 250, 194-199 10.1038/250194a0
40. Rane, M. J. and Calvo, K. C. (1997) Reversal of the nucleotide specificity of ketol acid reductoisomerase by site-directed mutagenesis identifies the NADPH binding site Arch. Biochem. Biophys. 338, 83-89 10.1006/abbi.1996.9802
41. Liang, L., Zhang, J. Q., and Lin, Z. L. (2007) Altering coenzyme specificity of Pichia stipitis xylose reductase by the semi-rational approach CASTing Microb. Cell Fact. 6, 36 10.1186/1475-2859-6-36
42. Zeng, Q.-K., Du, H.-L., Wang, J.-F., Wei, D.-Q., Wang, X.-N., Li, Y.-X., and Lin, Y. (2009) Reversal of coenzyme specificity and improvement of catalytic efficiency of Pichia stipitis xylose reductase by rational site-directed mutagenesis Biotechnol. Lett. 31, 1025-1029 10.1007/s10529-009-9980-x
43. Maurer, S. C., Kühnel, K., Kaysser, L. A., Eiben, S., Schmid, R. D., and Urlacher, V. B. (2005) Catalytic hydroxylation in biphasic systems using CYP102A1 mutants Adv. Synth. Catal. 347, 1090-1098 10.1002/adsc.200505044
44. Fasan, R., Crook, N. C., Peters, M. W., Meinhold, P., Buelter, T., Landwehr, M., Cirino, P. C., and Arnold, F. H. (2011) Improved product-per-glucose yields in P450-dependent propane biotransformations using engineered Escherichia coli Biotechnol. Bioeng. 108, 500-510 10.1002/bit.22984
45. Lee, J. K., Koo, B. S., and Kim, S. Y. (2003) Cloning and characterization of the xyl1 gene, encoding an NADH-preferring xylose reductase from Candida parapsilosis, and its functional expression in Candida tropicalis Appl. Environ. Microbiol. 69, 6179-6188 10.1128/AEM.69.10.6179-6188.2003
46. Cahn, J. K. B. (2016) Discovery of an NAD-preferring xylose reductase. In Engineering, Predicting, and Understanding Nicotinamide Cofactor Specificity, pp 45-55, California Institute of Technology, California.
47. Tóth-Petróczy, á. and Tawfik, D. S. (2013) Protein insertions and deletions enabled by neutral roaming in sequence space Mol. Biol. Evol. 30, 761-771 10.1093/molbev/mst003
48. Hamelryck, T. and Manderick, B. (2003) PDB file parser and structure class implemented in Python Bioinformatics 19, 2308-2310 10.1093/bioinformatics/btg299
49. Firth, A. E. and Patrick, W. M. (2008) GLUE-IT and PEDEL-AA: New programmes for analyzing protein diversity in randomized libraries Nucleic Acids Res. 36, W281-285 10.1093/nar/gkn226
50. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling Bioinformatics 22, 195-201 10.1093/bioinformatics/bti770
51. Schrodinger, L. L. C. (2010) The PyMOL Molecular Graphics System, Version 1.3r1, Schrödinger, LLC.
52. Gibson, D. G. (2011) Enzymatic assembly of overlapping DNA fragments, in Methods in Enzymology (Christopher, V., Ed.), pp 349-361, Academic Press.
53. Engqvist, M. K. M., McIsaac, R. S., Dollinger, P., Flytzanis, N. C., Abrams, M., Schor, S., and Arnold, F. H. (2015) Directed evolution of Gloeobacter violaceus rhodopsin spectral properties J. Mol. Biol. 427, 205-220 10.1016/j.jmb.2014.06.015