Purification and characterization of the epoxidase catalyzing the formation of fosfomycin from Pseudomonas syringae

Biochemistry

Volumn 47, Issue 33, 2008, Pages 8726-8735

  Munos, Jeffrey W ^a,c   Moon, Sung Ju ^a,d   Mansoorabadi, Steven O ^a   Chang, Weichen ^a   Hong, Lin ^a,e   Yan, Feng ^a,f   Liu, Aimin ^b   Liu, Hung Wen ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d IMMUNOMEDICS INC   (United States)

^e GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; AMINO ACIDS; ANTIBIOTICS; BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; CHEMICAL BONDS; CHEMICAL REACTIONS; DENSITY FUNCTIONAL THEORY; DEUTERIUM; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYMES; FOOD ADDITIVES; GENE ENCODING; HYDROGEN; IRON; METAL REFINING; METALS; NONMETALS; ORGANIC ACIDS; OXYGEN; PARAMAGNETIC RESONANCE; PORPHYRINS; PROBABILITY DENSITY FUNCTION; PURIFICATION; RATE CONSTANTS;

ACTIVE SITES; AMINO-ACID SEQUENCES; BOND DISSOCIATION ENERGIES; DENSITY FUNCTIONAL THEORY CALCULATIONS; ENCODING GENES; EPR SPECTROSCOPY; FE (II); FOSFOMYCIN; HEME IRON; HYDROGEN ATOMS; KINETIC EFFECTS; LOW DEGREE; METAL CENTERS; PSEUDOMONAS SYRINGAE; RATE-DETERMINING STEP; SECONDARY ALCOHOLS; SEQUENCE-HOMOLOGY; SPIN PROBES;

MOLECULAR OXYGEN;

2 HYDROXYPROPYLPHOSPHONIC ACID EPOXIDASE; 2 OXOPROPYLPHOSPHONIC ACID; ALCOHOL; DEUTERIUM; ENZYME; FOSFOMYCIN; HYDROGEN; IRON; NITRIC OXIDE; OXYGEN; PHOSPHONIC ACID DERIVATIVE;

AMINO ACID SEQUENCE; ARTICLE; DEHYDROGENATION; DENSITY FUNCTIONAL THEORY; ELECTRON SPIN RESONANCE; EPOXIDATION; HYDROXYLATION; OXIDATION; PRIORITY JOURNAL; PSEUDOMONAS SYRINGAE;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; FLAVIN MONONUCLEOTIDE; FOSFOMYCIN; GENE EXPRESSION REGULATION, BACTERIAL; IRON; MOLECULAR SEQUENCE DATA; NAD; OXIDOREDUCTASES; OXYGEN; PSEUDOMONAS SYRINGAE;

PSEUDOMONAS SYRINGAE; STREPTOMYCES WEDMORENSIS;

EID: 49749099580     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800877v     Document Type: Article

References (48)

1. Itoh, N., Kusaka, M., Hirota, T., and Nomura, A. (1995) Microbial production of antibiotic fosfomycin by a stereoselective epoxidation and its formation mechanism. Appl. Microbiol. Biotechnol. 43, 394-401.
2. Stengel, D., Gorzer, E., Schintler, M., Legat, F. J., Amann, W., Pieber, T., Ekkernkamp, A., and Graninger, W. (2005) Second-line treatment of limb-threatening diabetic foot infections with intravenous fosfomycin. J. Chemother. 17, 527-535.
3. Ko, K. S., Suh, J. Y., Peck, K. R., Lee, M. Y., Oh, W. S., Kwon, K. T., Jung, D. S., Lee, N. Y., and Song, J. H. (2007) In vitro activity of fosfomycin against ciprofloxacin-resistant or extended-spectrum β-lactamase-producing Escherichia coli isolated from urine and blood. Diagn. Microbiol. Infect. Dis. 58, 111-115.
4. Nakazawa, H., Kikuchi, Y., Honda, T., Isago, T., and Nozaki, M. (2003) Enhancement of antimicrobial effects of various antibiotics against methicillin-resistant Staphylococcus aureus (MRSA) by combination with fosfomycin. J. Infect. Chemother. 9, 304-309.
5. Cassone, M., Campanile, F., Pantosti, A., Venditti, M., and Stefani, S. (2004) Identification of a variant "Rome clone" of methicillin-resistant Staphylococcus aureus with decreased susceptibility to vancomycin, responsible for an outbreak in an intensive care unit. Microb. Drug Resist. 10, 43-49.
6. Marquardt, J. L., Brown, E. D., Lane, W. S., Haley, T. M., Ichikawa, Y., Wong, C. H., and Walsh, C. T. (1994) Kinetics, stoichiometry, and identification of the reactive thiolate in the inactivation of UDP-GlcNAc enolpyruvoyl transferase by the antibiotic fosfomycin. Biochemistry 33, 10646-10651.
7. Brown, E. D., Vivas, E. I., Walsh, C. T., and Kolter, R. (1995) MurA (MurZ), the enzyme that catalyzes the first committed step in peptidoglycan biosynthesis, is essential in Escherichia coli. J. Bacteriol. 177, 4194-4197.
8. Seto, H., and Kuzuyama, T. (1999) Bioactive natural products with carbon-phosphorus bonds and their biosynthesis. Nat. Prod. Rep. 16, 589-596.
9. Hidaka, T., Iwakura, H., Imai, S., and Seto, H. (1992) Studies on the biosynthesis of fosfomycin. 3. Detection of phosphoenolpyruvate phosphomutase activity in a fosfomycin high-producing strain of Streptomyces wedmorensis and characterization of its blocked mutant NP-7. J. Antibiot. 45, 1008-1010.
10. Jomaa, H., Wiesner, J., Sanderbrand, S., Altincicek, B., Weidemeyer, C., Hintz, M., Turbachova, I., Eberl, M., Zeidler, J., Lichtenthaler, H. K., Soldati, D., and Beck, E. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285, 1573-1576.
11. Hidaka, T., Mori, M., Imai, S., Hara, O., Nagaoka, K., and Seto, H. (1989) Studies on the biosynthesis of bialaphos (SF-1293). 9. Biochemical mechanism of C-P bond formation in bialaphos: Discovery of phosphoenolpyruvate phosphomutase which catalyzes the formation of phosphonopyruvate from phosphoenolpyruvate. J. Antibiot. 42, 491-494.
12. Seidel, H. M., Freeman, S., Seto, H., and Knowles, J. R. (1988) Phosphonate biosynthesis: Isolation of the enzyme responsible for the formation of a carbon-phosphorus bond. Nature 335, 457-458.
13. Kim, J., and Dunaway-Mariano, D. (1996) Phosphoenolpyruvate mutase catalysis of phosphoryl transfer in phosphoenolpyruvate: Kinetics and mechanism of phosphorus-carbon bond formation. Biochemistry 35, 4628-4635.
14. Liu, S., Lu, Z., Jia, Y., Dunaway-Mariano, D., and Herzberg, O. (2002) Dissociative phosphoryl transfer in PEP mutase catalysis: Structure of the enzyme/sulfopyruvate complex and kinetic properties of mutants. Biochemistry 41, 10270-10276.
15. Nakashita, H., Watanabe, K., Hara, O., Hidaka, T., and Seto, H. (1997) Studies on the biosynthesis of bialaphos. Biochemical mechanism of C-P bond formation: Discovery of phosphonopyruvate decarboxylase which catalyzes the formation of phosphonoacetaldehyde from phosphonopyruvate. J. Antibiot. 50, 212-219.
16. Woodyer, R. D., Li, G., Zhao, H., and van der Donk, W. A. (2007) New insight into the mechanism of methyl transfer during the biosynthesis of fosfomycin. Chem. Commun., 359-361.
17. Liu, P., Murakami, K., Seki, T., He, X., Yeung, S. M., Kuzuyama, T., Seto, H., and Liu, H.-w. (2001) Protein purification and function assignment of the epoxidase catalyzing the formation of fosfomycin. J. Am. Chem. Soc. 123, 4619-4620.
18. Liu, P., Liu, A., Yan, F., Wolfe, M. D., Lipscomb, J. D., and Liu, H.-w. (2003) Biochemical and spectroscopic studies on (S)-2-hydroxypropylphosphonic acid epoxidase: A novel mononuclear non-heme iron enzyme. Biochemistry 42, 11577-11586.
19. Sono, M., Roach, M. P., Coulter, E. D., and Dawson, J. H. (1996) Heme-Containing Oxygenases. Chem. Rev. 96, 2841-2888.
20. Ortiz de Montellano, P. R. (1995) Cytochrome P450: Structure, Mechanism, and Biochemistry, 2nd ed., Plenum, New York.
21. Lange, S. J., and Que, L., Jr. (1998) Oxygen activating nonheme iron enzymes. Curr. Opin. Chem. Biol. 2, 159-172.
22. Kuzuyama, T., Seki, T., Kobayashi, S., Hidaka, T., and Seto, H. (1999) Cloning and expression in Escherichia coli of 2-hydroxypropylphosphonic acid epoxidase from the fosfomycin-producing organism, Pseudomonas syringae PB-5123. Biosci., Biotechnol., Biochem. 63, 2222-2224.
23. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
24. 18O]hydroxypropyl) phosphonic acid. Monatsh. Chem. 122, 389-398.
25. Woschek, A., Wuggenig, F., Peti, W., and Hammerschmidt, F. (2002) On the transformation of (S)-2-hydroxypropylphosphonic acid into fosfomycin in Streptomyces fradiae: A unique method of epoxide ring formation. ChemBioChem 3, 829-835.
26. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
27. Andrews, P. (1964) Estimation of the molecular weights of proteins by Sephadex gel-filtration. Biochem. J. 91, 222-233.
28. Fish, W. W. (1988) Rapid colorimetric micromethod for the quantitation of complexed iron in biological smaples. Methods Enzymol. 158, 357-364.
29. Paz, M. A., Fluckiger, R., Boak, A., Kagan, H. M., and Gallop, P. M. (1991) Specific detection of quinoproteins by redox-cycling staining. J. Biol. Chem. 266, 689-692.
30. Liu, P., Mehn, M. P., Yan, F., Zhao, Z., Que, L., Jr., and Liu, H.-w. (2004) Oxygenase activity in the self-hydroxylation of (S)-2- hydroxypropylphosphonic acid epoxidase involved in fosfomycin biosynthesis. J. Am. Chem. Soc. 126, 10306-10312.
31. Yan, F., Munos, J. W., Liu, P., and Liu, H.-w. (2006) Biosynthesis of fosfomycin, re-examination and re-confirmation of a unique Fe(II)- and NAD(P)H-dependent epoxidation reaction. Biochemistry 45, 11473-11481.
32. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Jr., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Baboul, A. G., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Gonzalez, C., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Andres, J. L., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian98, Gaussian, Inc., Pittsburgh, PA.
33. Higgins, L. J., Yan, F., Liu, P., Liu, H.-w., and Drennan, C. L. (2005) Structural insight into antibiotic fosfomycin biosynthesis by a mononuclear iron enzyme. Nature 437, 838-844.
34. Andersson, M. P., and Uvdal, P. (2005) New scale factors for harmonic vibrational frequencies using the B3LYP density functional method with the triple-ζ basis set 6-311+G(d,p). J. Phys. Chem. A 109, 2937-2941.
35. 15N]Histidine- Enriched Enzyme and a Molecular Orbital Interpretation. J. Am. Chem. Soc. 118, 8692-8699.
36. Yan, F., Li, T., Lipscomb, J. D., Liu, A., and Liu, H.-w. (2005) Site-directed mutagenesis and spectroscopic studies of the iron-binding site of (S)-2-hydroxypropylphosphonic acid epoxidase. Arch. Biochem. Biophys. 442, 82-91.
37. Zhao, Z., Liu, P., Murakami, K., Kuzuyama, T., Seto, H., and Liu, H.-w. (2002) Mechanistic studies of HPP epoxidase: Configuration of the substrate governs its enzymatic fate. Angew. Chem., Int. Ed. 41, 4529-4532.
38. Hammerschmidt, F. (1991) Biosynthesis of natural products with a phosphorus-carbon bond. Part 8. On the origin of the oxirane oxygen atom of fosformycin in Streptomyces fradiae. J. Chem. Soc., Perkin Trans. 8, 1993-1996.
39. 17O- enriched substrates and substrate analogues. Biochemistry 46, 12628-12638.
40. Solomon, E. I., Brunold, T. C., Davis, M. I., Kemsley, J. N., Lee, S. K., Lehnert, N., Neese, F., Skulan, A. J., Yang, Y. S., and Zhou, J. (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes. Chem. Rev. 100, 235-350.
41. Costas, M., Mehn, M. P., Jensen, M. P., and Que, L., Jr. (2004) Dioxygen activation at mononuclear nonheme iron active sites: Enzymes, models, and intermediates. Chem. Rev. 104, 939-986.
42. Baldwin, J. E., and Bradley, M. (1990) Isopenicillin N synthase: Mechanistic studies. Chem. Rev. 90, 1079-1088.
43. 8 complexes of isopenicillin N synthase: Substrate determination of oxidase versus oxygenase activity in nonheme Fe enzymes. J. Am. Chem. Soc. 129, 7427-7438.
44. Price, J. C., Barr, E. W., Tirupati, B., Bollinger, J. M., Jr., and Krebs, C. (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an α-ketoglutarate-dependent dioxygenase: A high-spin FeIV complex in taurine/α-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 42, 7497-7508.
45. Eser, B. E., Barr, E. W., Frantom, P. A., Saleh, L., Bollinger, J. M., Jr., Krebs, C., and Fitzpatrick, P. F. (2007) Direct Spectroscopic Evidence for a High-Spin Fe(IV) Intermediate in Tyrosine Hydroxylase. J. Am. Chem. Soc. 129, 11334-11335.
46. Koehntop, K. D., Emerson, J. P., and Que, L., Jr. (2005) The 2-His-1-carboxylate facial triad: A versatile platform for dioxygen activation by mononuclear non-heme iron(II) enzymes. J. Biol. lnorg. Chem. 10, 87-93.
47. Hashimoto, T., Matsuda, J., and Yamada, Y. (1993) Two-step epoxidation of hyoscyamine to scopolamine is catalyzed by bifunctional hyoscyamine 6β-hydroxylase. FEBS Lett. 329, 35-39.
48. Busby, R. W., and Townsend, C. A. (1996) A single monomeric iron center in clavaminate synthase catalyzes three nonsuccessive oxidative transformations. Bioorg. Med. Chem. 4, 1059-1064.