An efficient, multiply promiscuous hydrolase in the alkaline phosphatase superfamily

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 7, 2010, Pages 2740-2745

  Van Loo, Bert ^a   Jonas, Stefanie ^a   Babtie, Ann C ^a   Benjdia, Alhosna ^b   Berteau, Olivier ^b   Hyvönen, Marko ^a   Hollfelder, Florian ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CEMAGREF   (France)

Author keywords

Catalytic promiscuity; Evolution; Mechanism; Sulfatase; Superfamily

Indexed keywords

ALKALINE PHOSPHATASE; HYDROLASE; PMH ENZYME; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME REACTIVATION; ENZYME STRUCTURE; GENE DUPLICATION; GENE MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION;

ALKALINE PHOSPHATASE; BURKHOLDERIA; CATALYSIS; CATALYTIC DOMAIN; CHROMATOGRAPHY, GEL; EVOLUTION, MOLECULAR; HYDROGEN-ION CONCENTRATION; HYDROLASES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTATION; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 77649239492     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0903951107     Document Type: Article

References (36)

1. O'Brien PJ, Herschlag D (1999) Catalytic promiscuity and the evolution of new enzymatic activities. Chem Biol, 6:R91-R105.
2. Khersonsky O, Roodveldt C, Tawfik DS (2006) Enzyme promiscuity: evolutionary and mechanistic aspects. Curr Opin Chem Biol, 10:498-508.
3. Jonas S, Hollfelder F (2008) Mechanism and Catalytic Promiscuity: Emerging Mechanistic Principles for Identification and Manipulation of Catalytically Promiscuous Enzymes. Handbook of Protein Engineering, , ed Bornscheuer U (Wiley VCH, Weinheim, Germany), Vol 1, pp 47-79.
4. Glasner ME, Gerlt JA, Babbitt PC (2006) Evolution of enzyme superfamilies. Curr Opin Chem Biol, 10:492-497.
5. Aharoni A, et al. (2005) The 'evolvability' of promiscuous protein functions. Nat Genet, 37:73-76.
6. Jensen RA (1976) Enzyme recruitment in evolution of new function. Annu Rev Microbiol, 30:409-425.
7. Hughes AL (1994) The evolution of functionally novel proteins after gene duplication. Proc Biol Sci, 256:119-124.
8. Patrick WM, Matsumura I (2008) A study in molecular contingency: Glutamine phosphoribosylpyrophosphate amidotransferase is a promiscuous and evolvable phosphoribosylanthranilate isomerase. J Mol Biol, 377:323-336.
9. Dotson SB, Smith CE, Ling CS, Barry GF, Kishore GM (1996) Identification, characterization, and cloning of a phosphonate monoester hydrolase from Burkholderia caryophilli PG2982. J Biol Chem, 271:25754-25761.
10. Schmidt B, Selmer T, Ingendoh A, von Figura K (1995) A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell, 82:271-278.
11. Jonas S, van Loo B, Hyvonen M, Hollfelder F (2008) A new member of the alkaline phosphatase superfamily with a formylglycine nucleophile: Structural and kinetic characterisation of a phosphonate monoester hydrolase/ phosphodiesterase from Rhizobium leguminosarum. J Mol Biol, 384:120-136.
12. Hanson SR, Best MD, Wong C-H (2004) Sulfatases: Structure, mechanism, biological activity, inhibition, and synthetic utility. Angew Chem Int Ed, 43:5736-5763.
13. Galperin MY, Bairoch A, Koonin EV (1998) A superfamily of metalloenzymes unifies phosphopentomutase and cofactor-independent phosphoglycerate mutase with alkaline phosphatases and sulfatases. Protein Sci, 7:1829-1835.
14. Babtie AC, Bandyopadhyay S, Olguin LF, Hollfelder F (2009) Efficient catalytic promiscuity for chemically distinct reactions. Angew Chem Int Ed, 48:3692-3694.
15. Lassila JK, Herschlag D (2008) Promiscuous sulfatase activity and thio-effects in a phosphodiesterase of the alkaline phosphatase superfamily. Biochemistry, 47:12853-12859.
16. O'Brien PJ, Herschlag D (1998) Sulfatase activity of E. coli alkaline phosphatase demonstrates a functional link to arylsulfatases, an evolutionary related enzyme family. J Am Chem Soc, 120:12369-12370.
17. O'Brien PJ, Herschlag D (2001) Functional interrelationships in the alkaline phosphatase superfamily: Phosphodiesterase activity of Escherichia coli alkaline phosphatase. Biochemistry, 40:5691-5699.
18. 13 for phosphate monoester hydrolysis. J Am Chem Soc, 130:16547-16555.
19. Zalatan JG, Fenn TD, Brunger AT, Herschlag D (2006) Structural and functional comparisons of nucleotide pyrophosphatase/phosphodiesterase and alkaline phosphatase: Implications for mechanism and evolution. Biochemistry, 45:9788-9803.
20. Peng J, Schmidt B, von Figura K, Dierks T (2002) Identification of formylglycine in sulfatases by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J Mass Spectrom, 38:80-86.
21. Carrico IS, Carlson BL, Bertozzi CR (2007) Introducing genetically encoded aldehydes into proteins. Nat Chem Biol, 3:321-322.
22. Benjdia A, Deho G, Rabot S, Berteau O (2007) First evidences for a third sulfatase maturation system in prokaryotes from E. coli aslB and ydeM deletion mutants. FEBS Lett, 581:1009-1014.
23. Lee B, Richards FM (1971) The interpretation of protein structures: Estimation of static accessibility. J Mol Biol, 55:379-400.
24. Garcia De La Torre J, Huertas ML, Carrasco B (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys J, 78:719-730.
25. Shenoy AR, Sreenath N, Podobnik M, Kovacevic M, Visweswariah SS (2005) The Rv0805 gene from Mycobacterium tuberculosis encodes a 3′ , 5′-cyclic nucleotide phosphodiesterase: biochemical and mutational analysis. Biochemistry, 44:15695-15704.
26. Ghanem E, Li Y, Xu C, Raushel FM (2007) Characterization of a phosphodiesterase capable of hydrolyzing EA 2192, the most toxic degradation product of the nerve agent VX. Biochemistry, 46:9032-9040.
27. Wolfenden R (2006) Degrees of difficulty of water-consuming reactions in the absence of enzymes. Chem Rev, 106:3379-3396.
28. Kuusela S, Lönnberg H (1993) Metal ions that promote the hydrolysis of nucleoside phosphoesters do not enhance intramolecular phosphate migration. J Phys Org Chem, 6:347-356.
29. Morrow JR, Iranzo O (2004) Synthetic metallonucleases for RNA cleavage. Curr Opin Chem Biol, 8:192-200.
30. Feng G, Mareque-Rivas JC, Torres Martin de Rosales R, Williams NH (2005) A highly reactive mononuclear Zn(II) complex for phosphodiester cleavage. J Am Chem Soc, 127:13470-13471.
31. Peracchi A (2001) Enzyme catalysis: Removing chemically 'essential' residues by site-directed mutagenesis. Trends Biochem Sci, 26:497-503.
32. Menger FM, Ladika M (1987) Origin of rate accelerations in an enzyme model: The p-nitrophenyl ester syndrome. J Am Chem Soc, 109:3145-3146.
33. Zalatan JG, Herschlag D (2006) Alkaline phosphatase mono- and diesterase reactions: Comparative transition state analysis. J Am Chem Soc, 128:1293-1303.
34. Yang K, Metcalf WW (2004) A new activity for an old enzyme: Escherichia coli bacterial alkaline phosphatase is a phosphite-dependent hydrogenase. Proc Natl Acad Sci USA, 101:7919-7924.
35. Toscano MD, Woycechowsky KJ, Hilvert D (2007) Minimalist active-site redesign: Teaching old enzymes new tricks. Angew Chem, Int Ed, 46:3212-3236.
36. McLoughlin SY, Jackson C, Liu JW, Ollis DL (2004) Growth of Escherichia coli coexpressing phosphotriesterase and glycerophosphodiester phosphodiesterase, using paraoxon as the sole phosphorus source. Appl Environ Microbiol, 70:404-412.