Mutagenesis of the phosphate-binding pocket of KDPG aldolase enhances selectivity for hydrophobic substrates

Protein Science

Volumn 16, Issue 11, 2007, Pages 2368-2377

  Cheriyan, Manoj ^a   Toone, Eric J ^b   Fierke, Carol A ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Active site; Aldolase; Biocatalysis; Directed evolution; KDPG; Nikkomycin; Protein engineering; Rational redesign; Substrate specificity

Indexed keywords

FRUCTOSE BISPHOSPHATE ALDOLASE; NIKKOMYCIN; PHOSPHATE BINDING PROTEIN;

ARTICLE; BIOCATALYST; CHEMICAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; MUTAGENESIS; PRIORITY JOURNAL;

ALDEHYDE-LYASES; AMINOGLYCOSIDES; BINDING SITES; CATALYSIS; ESCHERICHIA COLI; HYDRO-LYASES; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTAGENESIS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHATES; PROTEIN ENGINEERING; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI;

EID: 35648977174     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.073042907     Document Type: Article

References (34)

1. Allard, J., Grochulski, P., and Sygusch, J. 2001. Covalent intermediate trapped in 2-keto-3-deoxy-6-phosphogluconate (KDPG) aldolase structure at 1.95 Å resolution. Proc. Natl. Acad. Sci. 98: 3679-3684.
2. Chica, R.A., Doucet, N., and Pelletier, J.N. 2005. Semi-rational approaches to engineering enzyme activity: Combining the benefits of directed evolution and rational design. Curr. Opin. Biotechnol. 16: 378-384.
3. Copley, R.R. and Barton, G.J. 1994. A structural analysis of phosphate and sulphate binding sites in proteins. Estimation of propensities for binding and conservation of phosphate binding sites. J. Mol. Biol. 242: 321-329.
4. Cotterill, I.A., Shelton, M.C., Machemer, D.E., Henderson, D.P., and Toone, E.J. 1998. Effect of phosphorylation on the rate of unnatural electrophiles with KDPG aldolase. J. Chem. Soc. Perkin Trans. 1: 1335-1341.
5. DeSantis, G., Liu, J., Clark, D.P., Heine, A., Wilson, I.A., and Wong, C.H. 2003. Structure-based mutagenesis approaches toward expanding the substrate specificity of D-2-deoxyribose-5-phosphate aldolase. Bioorg. Med. Chem. 11: 43-52.
6. Fessner, W.D. and Walter, C. 1997. Enzymatic C-C bond formation in asymmetric synthesis. Top Cur Chem 184: 97-194.
7. Fong, S., Machajewski, T.D., Mak, C.C., and Wong, C.H. 2000. Directed evolution of D-2-keto-3-deoxy-6-phosphogluconate aldolase to new variants for the efficient synthesis of D- and L-sugars. Chem. Biol. 7: 873-883.
8. Franke, D., Hsu, C.C., and Wong, C.H. 2004. Directed evolution of aldolases. Methods Enzymol. 388: 224-238.
9. Fullerton, S.W.B., Griffiths, J.S., Merkel, A.B., Cheriyan, M., Wymer, N.J., Hutchins, M.J., Fierke, C.A., Toone, E.J., and Naismith, J.H. 2006. Mechanism of the class I KDPG aldolase. Bioorg. Med. Chem. 14: 3002-3010.
10. Geddie, M.L. and Matsumura, I. 2004. Rapid evolution of β-glucuronidase specificity by saturation mutagenesis of an active site loop. J. Biol. Chem. 279: 26462-26468.
11. Griffiths, J.S., Wymer, N.J., Njolito, E., Niranjanakumari, S., Fierke, C.A., and Toone, E.J. 2002. Cloning, isolation and characterization of the Thermotoga maritima KDPG aldolase. Bioorg. Med. Chem. 10: 545-550.
12. Griffiths, J.S., Cheriyan, M., Corbell, J.B., Pocivavsek, L., Fierke, C.A., and Toone, E.J. 2004. A bacterial selection for the directed evolution of pyruvate aldolases. Bioorg. Med. Chem. 12: 4067-4074.
13. Henderson, D.P., Shelton, M.C., Cotterill, I.A., and Toone, E.J. 1997. Stereospecific preparation of the N-terminal amino acid moiety of nikkomycins Kx and Kz via a multiple enzyme substrate. J. Org. Chem. 62: 7910-7911.
14. Henderson, D.P., Cotterill, I.C., Shelton, M.C., and Toone, E.J. 1998. 2-keto-3-deoxy-6-phosphogalactonate aldolase as a catalyst for stereocontrolled carbon-carbon bond formation. J. Org. Chem. 63: 906-907.
15. Hsu, C.C., Hong, Z., Wada, M., Franke, D., and Wong, C.H. 2005. Directed evolution of D-sialic acid aldolase to L-3-deoxy-manno-2-octulosonic acid (L-KDO) aldolase. Proc. Natl. Acad. Sci. 102: 9122-9126.
16. Ingram, J.M. and Wood, W.A. 1966. The mechanism of 2-keto-3-deoxy-6- phosphogluconic aldolase. J. Biochem. 241: 3256-3261.
17. Karplus, P.A. 1997. Hydrophobicity regained. Protein Sci. 6: 1302-1307.
18. Kinoshita, K., Sadanami, K., Kidera, A., and Go, N. 1999. Structural motif of phosphate-binding site common to various protein superfamilies: All-against-all structural comparison of protein-mononucleotide complexes. Protein Eng. 12: 11-14.
19. Mavridis, I.M., Hatada, M.H., Tulinsky, A., and Lebioda, L. 1982. Structure of 2-keto-3-deoxy-6-phosphogluconate aldolase at 2.8 Å resolution. J. Mol. Biol. 162: 419-444.
20. Michaelis, L. and Menten, M.L. 1913. Die knetik der invertinwirkung. Biochem. Z. 49: 333-369.
21. Midelfort, C.F., Gupta, R.K., and Meloche, H.P. 1977. Specificity of 2-keto-3-deoxygluconate-6-P aldolase for open chain form of 2-keto-3- deoxygluconate-6-P. J. Biochem. 252: 3486-3492.
22. Morley, K.L. and Kazlauskas, R.J. 2005. Improving enzyme properties: When are closer mutations better? Trends Biotechnol. 23: 231-237.
23. Nagano, N., Orengo, C.A., and Thornton, J.M. 2002. One fold with many functions: The evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 321: 741-765.
24. O'Connell, E.L. and Meloche, H.P. 1982. Enzymic synthesis of 2-keto-3-deoxygluconate-6-phosphate using 6-phosphogluconate dehydratase. Methods Enzymol. 89: 98-101.
25. Parikh, M.R. and Matsumura, I. 2005. Site-saturation mutagenesis is more efficient than DNA shuffling for the directed evolution of β-fucosidase from β-galactosidase. J. Mol. Biol. 352: 621-628.
26. Peekhaus, N. and Conway, T. 1998. What's for dinner?: Enter-Doudoroff metabolism in Eschericha coli. J. Bacteriol. 180: 3495-3502.
27. Ran, N. and Frost, J.W. 2007. Directed evolution of 2-keto-3-deoxy-6- phosphogalactonate aldolase to replace 3-deoxy-D-arabino-heptulosonic acid 7-phosphate synthase. J. Am. Chem. Soc. 129: 6130-6139.
28. Sambrook, J. and Russell, D.W. 2001. Molecular cloning: A laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
29. Samland, A.K. and Sprenger, G.A. 2006. Microbial aldolases as C-C bonding enzymes - Unknown treasures and new developments. Appl. Microbiol. Biotechnol. 71: 253-264.
30. Schlüter, U. 1982. Ultrastructural evidence for inhibition of chitin synthesis by nikkomycin. Dev. Genes Evol. 91: 205-207.
31. Shelton, M.C., Cotterill, I.C., Novak, S.T., Poonawala, R.M., Sudarshan, S., and Toone, E.J. 1996. 2-keto-3-deoxy-6-phosphogluconate aldolases as catalysts for stereocontrolled carbon-carbon bond formation. J. Am. Chem. Soc. 118: 2117-2125.
32. Wada, M., Hsu, C.C., Franke, D., Mitchell, M., Heine, A., Wilson, I., and Wong, C.H. 2003. Directed evolution of N-acetylneuraminic acid aldolase to catalyze enantiomeric aldol reactions. Bioorg. Med. Chem. 11: 2091-2098.
33. Wilmanns, M., Hyde, C.C., Davies, D.R., Kirschner, K., and Jansonius, J.N. 1991. Structural conservation in parallel β/α-barrel enzymes that catalyze three sequential reactions in the pathway of tryptophan biosynthesis. Biochemistry 30: 9161-9169.
34. Wymer, N., Buchanan, L.V., Henderson, D., Mehta, N., Botting, C.H., Pocivavsek, L., Fierke, C.A., Toone, E.J., and Naismith, J.H. 2001. Directed evolution of a new catalytic site in 2-keto-3-deoxy-6-phosphogluconate aldolase from Escherichia coli. Structure 9: 1-9.