Catalytic, noncatalytic, and inhibitory phenomena: Kinetic analysis of (4-hydroxyphenyl)pyruvate dioxygenase from Arabidopsis thaliana

Biochemistry

Volumn 45, Issue 19, 2006, Pages 6044-6055

  Purpero, Vincent M ^a   Moran, Graham R ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; MASS SPECTROMETRY; METABOLISM; MICROORGANISMS; MOLECULAR DYNAMICS; PLANTS (BOTANY); REACTION KINETICS; STOICHIOMETRY;

(4-HYDROXYPHENYL)PYRUVATE DIOXYGENASE (HPPD); CATABOLISM DEFECTS; MAMMALIAN METABOLISM; STREPTOMYCES;

ENZYMES;

4 HYDROXYPHENYLPYRUVATE DIOXYGENASE; 4 HYDROXYPHENYLPYRUVIC ACID; HOMOGENTISIC ACID; OXYGEN; PHENYLACETIC ACID; PLASTOQUINONE; PYRUVIC ACID DERIVATIVE; TOCOPHEROL; TYROSINE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CATALYSIS; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME KINETICS; ENZYME METABOLISM; ENZYME PURIFICATION; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOICHIOMETRY;

4-HYDROXYPHENYLPYRUVATE DIOXYGENASE; ARABIDOPSIS; CATALYSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; KINETICS; RECOMBINANT PROTEINS;

ARABIDOPSIS THALIANA; MAMMALIA; STREPTOMYCES;

EID: 33646537847     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052409c     Document Type: Article

References (63)

1. Hausinger, R. P. (2004) FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes, Crit. Rev. Biochem. Mol. Biol. 39, 21-68.
2. Serre, L., Sailland, A., Sy, D., Boudec, P., Rolland, A., Pebay-Peyroula, E., and Cohen-Addad, C. (1999) Crystal structure of Pseudomonas fluorescens 4-hydroxyphenylpyruvate dioxygenase: an enzyme involved in the tyrosine degradation pathway, Structure Fold Des. 7, 977-988.
3. Neidig, M. L., Kavana, M., Moran, G. R., and Solomon, E. I. (2004) CD and MCD studies of the non-heme ferrous active site in (4-hydroxyphenyl)pyruvate dioxygenase: correlation between oxygen activation in the extradiol and alpha-KG dependent dioxygenases, J. Am. Chem. Soc. 126, 4486-4487.
4. Johnson-Winters, K., Purpero, V. M., Kavana, M., Nelson, T., and Moran, G. R. (2003) (4-Hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis: the basis for ordered substrate addition, Biochemistry 42, 2072-2080.
5. Moran, G. R. (2005) 4-Hydroxyphenylpyruvate dioxygenase, Arch. Biochem. Biophys. 433, 117-128.
6. Guroff, G., Daly, J. W., Jerina, D. M., Renson, J., Witkop, B., and Udenfriend, S. (1967) Hydroxylation-induced migration: the NIH shift, Science 157, 1524-1530.
7. Johnson-Winters, K., Purpero, V. M., Kavana, M., and Moran, G. R. (2005) Accumulation of multiple intermediates in the catalytic cycle of (4-hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis, Biochemistry 44, 7189-7199.
8. Lindstedt, S., Odelhog, B., and Rundgren, M. (1977) Purification and some properties of 4-hydroxyphenylpyruvate dioxygenase from Pseudomonas sp. P. J. 874, Biochemistry 16, 3369-3377.
9. Lindstedt, S., and Rundgren, M. (1982) Blue color, metal content, and substrate binding in 4-hydroxyphenylpyruvate dioxygenase from Pseudomonas sp. strain P. J. 874, J. Biol. Chem. 257, 11922-11931.
10. Lindblad, B., Lindstedt, G., Lindstedt, S., and Rundgren, M. (1977) Purification and some properties of human. 4-hydroxyphenylpyruvate dioxygenase (I), J. Biol. Chem. 252, 5073-5084.
11. Rundgren, M. (1977) Multiple forms of human 4-hydroxyphenylpyruvate dioxygenase (II), J. Biol. Chem. 252, 5085-5093.
12. Goodwin, B. L. (1972) Tyrosine Catabolism, Oxford University Press: New York.
13. Taniguchi, K., and Armstrong, M. D. (1963) The enzymatic formation of o-hydroxyphenylacetic acid, J. Biol. Chem. 238, 4091-4097.
14. Denum, J., Lindstedt, S., and Rundgren, M. (1982) in Oxidases and Related Redox Systems (King, T. E., Mason, H. S., and Morrison, M., Eds.) pp 519-542, Pergamon Press, Albany, NY.
15. Taniguchi, K., Kappe, T., and Armstrong, M. D. (1964) Further studies on phenylpyruvate oxidase occurrence of side chain rearrangement and comparison with p-hydroxyphenylpyruvate oxidase, J. Biol. Chem. 239, 3389-3395.
16. Lindstedt, S., and Rundgren, M. (1982) Inhibition of 4- hydroxyphenylpyruvate dioxygenase from Pseudomonas sp. strain P. J. 874 the enol tautomer of the substrate, Biochim. Biophys. Acta 704, 66-74.
17. Wada, G. H., Fellman, J. H., Fujita, T. S., and Roth, E. S. (1975) Purification and properties of avian liver p-hydroxyphenylpyruvate hydroxylase, J. Biol. Chem. 250, 6720-6726.
18. Rundgren, M. (1977) Steady-state kinetics of 4-hydroxyphenylpyruvate dioxygenase from human liver (III), J. Biol. Chem. 252, 5094-5099.
19. Goodwin, T. W., and Mercer, E. I. (1983) Introduction to Plant Biochemistry, 2nd ed., Pergamon Press, Sydney, Australia.
20. Hellyer, R. (1968) The occurrence of beta-triketones in the steam-volatile oils of some myrtaceous Australian plants, Aust. J. Chem. 21, 2825-2828.
21. Romagni, J. G., Meazza, G., Nanayakkara, N. P., and Dayan, F. E. (2000) The phytotoxic lichen metabolite, usnic acid, is a potent inhibitor of plant p-hydroxyphenylpyruvate dioxygenase, FEBS Lett. 480, 301-305.
22. Gray, R. A., Russay, R. J., and Tseng, C. K. US Patent (1980) pp 202, 840.
23. Mitchell, G., Bartlett, D. W., Fraser, T. E., Hawkes, T. R., Holt, D. C., Townson, J. K., and Wiehert, R. A. (2001) Mesotrione: a new selective herbicide for use in maize, Pest. Manag. Sci. 57, 120-128.
24. Schulz, A., Ort, O., Beyer, P., and Kleinig, H. (1993) SC-0051, a 2-benzoyl-cyclohexane-1,3-dione bleaching herbicide, is a potent inhibitor of the enzyme p-hydroxyphenylpyruvate dioxygenase, FEBS Lett 318, 162-166.
25. Michaely, W. J., and Kratz, G. W. (1988) U.S. Patent 780,127.
26. Hall, M. G., Wilks, M. F., Provan, W. M., Eksborg, S., and Lumholtz, B. (2001) Pharmacokinetics and pharmacodynamics of NTBC (2-(2-nitro-4- fluoromethylbenzoyl)-1,3-cyclohexanedione) and mesotrione, inhibitors of 4-hydroxyphenyl pyruvate dioxygenase (HPPD) following a single dose to healthy male volunteers, Br. J. Clin. Pharmacol. 52, 169-177.
27. Lindstedt, S., Holme, E., Lock, E. A., Hjalmarson, O., and Strandvik, B. (1992) Treatment of hereditary tyrosinaemia type I by inhibition of 4-hydroxyphenylpyruvate dioxygenase [see comments], Lancet 340, 813-817.
28. Garrod, E. A. (1902) The incidence of alkaptonuria: a study in clinical individuality, Lancet, 1616-1620.
29. Garrod, A. E. (1908) The croonian lectures on inborn errors of metabolism. Lecture II. Alkaptonuria, Lancet, 73-79.
30. Phornphutkul, C., Introne, W. J., Perry, M. B., Bernardini, I., Murphey, M. D., Fitzpatrick, D. L., Anderson, P. D., Huizing, M., Anikster, Y., Gerber, L. H., and Gahl, W. A. (2002) Natural history of alkaptonuria, N. Engl. J. Med. 347, 2111-2121.
31. Suwannarat, P., O'Brien, K., Perry, M. B., Sebring, N., Bernardini, I., Kaiser-Kupfer, M. I., Rubin, B. I., Tsilou, E., Gerber, L. H., and Gahl, W. A. (2005) Use of nitisinone in patients with alkaptonuria, Metabolism 54, 719-728.
32. Secor, J. (1994) Inhibition of barnyardgrass 4-hydroxyphenylpyruvate dioxygenase by sulcotrione, Plant Physiol. 106, 1429-1433.
33. Pallett, K. E., Cramp, S. M., Little, J. P., Veerasekaran, P., Crudace, A. J., and Slater, A. E. (2001) Isoxaflutole: the background to its discovery and the basis of its herbicidal properties, Pest. Manag. Sci. 57, 133-142.
34. Kavana, M., and Moran, G. R. (2003) Interaction of (4-hydroxyphenyl) pyruvate dioxygenase with the specific inhibitor 2-[2-nitro-4-(trifluoromethyl) benzoyl]-1,3-cyclohexanedione, Biochemistry 42, 10238-10245.
35. Brownlee, J., Kayunta, J.-W., Harrison, D. H. T., and Moran, G. R. (2004) The structure of the ferrous form of (4-hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis in complex with the therapeutic herbicide, NTBC, Biochemistry 43, 6370-6377.
36. Studier, F. W., and Moffatt, B. A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes, J. Mol. Biol. 189, 113-130.
37. Norris, S. R., Shen, X. H., and DellaPenna, D. (1998) Complementation of the Arabidopsis pds1 mutation with the gene encoding p-hydroxyphenylpyruvate dioxygenase, Plant Physiol. 117, 1317-1323.
38. Yang, C., Pflugrath, J. W., Camper, D. L., Foster, M. L., Pernich, D. J., and Walsh, T. A. (2004) Structural basis for herbicidal inhibitor selectivity revealed by comparison of crystal structures of plant and mammalian 4-hydroxyphenylpyruvate dioxygenases, Biochemistry 43, 10414-10423.
39. Pace, N. C., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein, Protein Sci. 4, 2411-2423.
40. Patrie, S. M., Charlebois, J. P., Whipple, D., Kelleher, N. L., Hendrickson, C. L., Quinn, J. P., Marshall, A. G., and Mukhopadhyay, B. (2004) Construction of a hybrid quadrupole/Fourier transform ion cyclotron resonance mass spectrometer for versatile MS/MS above 10 kDa, J. Am. Soc. Mass Spectrom. 15, 1099-1108.
41. Senko, M. W., Canterbury, J. D., Guan, S., and Marshall, A. G. (1996) A high-performance modular data system for Fourier transform ion cyclotron resonance mass spectrometry, Rapid Commun. Mass Spectrom. 10, 1839-1844.
42. Grabski, A., Mehler, M., and Drott, D. (2003), innovations (Novagen), 1-6.
43. Lederer, B., and Boger, P. (2005) Recombinant p-hydroxyphenylpyruvate dioxygenase of high activity, Z. Naturforsch., C: Biosci. 60, 549-556.
44. Roche, P. A., Moorehead, T. J., and Hamilton, G. A. (1982) Purification and properties of hog liver 4-hydroxyphenylpyruvate dioxygenase, Arch. Biochem. Biophys. 216, 62-73.
45. Copik, A. J., Waterson, S., Swierczek, S. I., Bennett, B., and Holz, R. C. (2005) Both nucleophile and substrate bind to the catalytic Fe(II)-center in the type-II methionyl aminopeptidase from Pyrococcus furiosus, Inorg. Chem. 44, 1160-1162.
46. Narvaez, A. J., Kalman, L., LoBrutto, R., Allen, J. P., and Williams, J. C. (2002) Influence of the protein environment on the properties of a tyrosyl radical in reaction centers from Rhodobacter sphaeroides, Biochemistry 41, 15253-15258.
47. Elleingand, E., Gerez, C., Un, S., Knupling, M., Lu, G., Salem, J., Rubin, H., Sauge-Merle, S., Laulhere, J. P., and Fontecave, M. (1998) Reactivity studies of the tyrosyl radical in ribonucleotide reductase from Mycobacterium tuberculosis and Arabidopsis thaliana-comparison with Escherichia coli and mouse, Eur. J. Biochem. 258, 485-490.
48. Svistunenko, D. A., Dunne, J., Fryer, M., Nicholls, P., Reeder, B. J., Wilson, M. T., Bigotti, M. G., Cutruzzola, F., and Cooper, C. E. (2002) Comparative study of tyrosine radicals in hemoglobin and myoglobins treated with hydrogen peroxide, Biophys. J. 83, 2845-2855.
49. Ryle, M. J., Liu, A., Muthukumaran, R. B., Ho, R. Y., Koehntop, K. D., McCracken, J., Que, L., Jr., and Hausinger, R. P. (2003) O2- and alpha-ketoglutarate-dependent tyrosyl radical formation in TauD, an alpha-keto acid-dependent non-heme iron dioxygenase, Biochemistry 42, 1854-1862.
50. Neidig, M. L., Decker, A., Kavana, M., Moran, G. R., and Solomon, E. I. (2005) Spectroscopic and computational studies of NTBC bound to the non-heme iron enzyme (4-hydroxyphenyl)pyruvate dioxygenase: Active site contributions to drug inhibition, Biochem. Biophys. Res. Commun. 338, 206-214.
51. Hager, S. E., Gregerman, R. I., and Knox, W. E. (1957) p-Hydroxyphenylpyruvate oxidase of liver, J. Biol. Chem. 225, 935-947.
52. Lindblad, B., Lindstedt, G., and Lindstedt, S. (1970) The Mechanism of enzymic formation of homogentisate from p-hydroxyphenylpyruvate, J. Am. Chem. Soc. 92, 7446-7449.
53. Rundgren, M. (1982) Tritium isotope effects in the reaction catalyzed by 4-hydroxyphenylpyruvate dioxygenase from Pseudomonas sp. strain P. J. 874, Biochim. Biophys. Acta 704, 59-65.
54. Lindblad, B., Lindstedt, S., and Steen, G. (1977) On the enzymic defects in hereditary tyrosinemia, Proc. Natl. Acad. Sci. U.S.A. 74, 4641-4645.
55. Beltran-Valero de Bernabe, D., Jimenez, F. J., Aquaron, R., and Rodriguez de Cordoba, S. (1999) Analysis of alkaptonuria (AKU) mutations and polymorphisms reveals that the CCC sequence motif is a mutational hot spot in the homogentisate 1,2 dioxygenase gene (HGO), Am. J. Hum. Genet. 64, 1316-1322.
56. Fernandez-Canon, J. M., Granadino, B., Beltran-Valero de Bernabe, D., Renedo, M., Fernandez-Ruiz, E., Penalva, M. A., and Rodriguez de Cordoba, S. (1996) The molecular basis of alkaptonuria, Nat. Genet. 14, 19-24.
57. Garcia, I., Job, D., and Matringe, M. (2000) Inhibition of p-hydroxyphenylpyruvate dioxygenase by the diketonitrile of isoxaflutole: a case of half-site reactivity, Biochemistry 39, 7501-7507.
58. Fritze, I. M., Linden, L., Freigang, J., Auerbach, G., Huber, R., and Steinbacher, S. (2004) The crystal structures of Zea mays and Arabidopsis 4-hydroxyphenylpyruvate dioxygenase, Plant Physiol. 134, 1388-400.
59. Kindl, H. (1969) Biosynthesis and metabolism of hydroxyphenylacetic acids in higher plants, Eur. J. Biochem. 7, 340-347.
60. Olivera, E. R., Minambres, B., Garcia, B., Muniz, C., Moreno, M. A., Ferrandez, A., Diaz, E., Garcia, J. L., and Luengo, J. M. (1998) Molecular characterization of the phenylacetic acid catabolic pathway in Pseudomonas putida U: the phenylacetyl-CoA catabolon, Proc. Natl. Acad. Sci. U.S.A. 95, 6419-6424.
61. Knappskog, P. M., Eiken, H. G., Martinez, A., Flatmark, T., and Apold, J. (1995) The PKU mutation S349P causes complete loss of catalytic activity in the recombinant phenylalanine hydroxylase enzyme, Hum. Genet. 95, 171-173.
62. Armstrong, M. D., Shaw, K. N., and Robinson, K. S. (1955) Studies on phenylketonuria. II. The excretion of o-hydroxyphenylacetic acid in phenylketonuria, J. Biol. Chem. 213, 797-804.
63. Dyson, J. S., Beulke, S., Brown, C. D., and Lane, M. C. (2002) Adsorption and degradation of the weak acid mesotrione in soil and environmental fate implications, J. Environ. Qual. 31, 613-618.