Evidence for a high-Spin Fe(IV) species in the catalytic cycle of a bacterial phenylalanine hydroxylase

Biochemistry

Volumn 50, Issue 11, 2011, Pages 1928-1933

  Panay, Aram Joel ^a   Lee, Michael ^b   Krebs, Carsten ^b   Bollinger, J Martin ^b   Fitzpatrick, Paul F ^c,d  

^a TEXAS A AND M UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c University of Texas Health Science Center   (United States)

^d UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC CYCLES; CHROMOBACTERIUM VIOLACEUM; DATA SETS; DIOXYGENS; ENZYME-SUBSTRATE COMPLEXES; HEME IRON; HYDROXYLASES; MOSSBAUER; PHENYLALANINE HYDROXYLASE; PRODUCT RELEASE; QUENCH METHODS; RATE LIMITING; SHORT REACTION TIME; TYROSINE HYDROXYLASE;

AMINO ACIDS; BACTERIOLOGY; CHEMICAL ANALYSIS; ENZYMES; HYDROXYLATION; MOLYBDENUM; OXYGEN; PORPHYRINS; RATE CONSTANTS;

REACTION INTERMEDIATES;

6 METHYLTETRAHYDROPTERIN; IRON; OXYGEN; PHENYLALANINE 4 MONOOXYGENASE; TYROSINE; TYROSINE 3 MONOOXYGENASE;

ARTICLE; CATALYSIS; CHEMICAL REACTION; CHROMOBACTERIUM VIOLACEUM; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME SUBSTRATE; HYDROXYLATION; MOSSBAUER SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL;

BINDING SITES; CATALYSIS; CHROMOBACTERIUM; IRON; KINETICS; OXYGEN; PHENYLALANINE HYDROXYLASE; PTERINS; SPECTROSCOPY, MOSSBAUER; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); CHROMOBACTERIUM VIOLACEUM;

EID: 79952783028     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1019868     Document Type: Article

References (46)

1. Fitzpatrick, P. F. (2000) The aromatic amino acid hydroxylases. In Advances in Enzymology and Related Areas of Molecular Biology (Purich, D. L., Ed.) pp 235 - 294, John Wiley & Sons, Inc., New York.
2. Eisensmith, R. C. and Woo, S. L. C. (1991) Phenylketonuria and the phenylalanine hydroxylase gene Mol. Biol. Med. 8, 3-18
3. Erlandsen, H., Kim, J. Y., Patch, M. G., Han, A., Volner, A., Abu-Omar, M. M., and Stevens, R. C. (2002) Structural comparison of bacterial and human iron-dependent phenylalanine hydroxylases: Similar fold, different stability and reaction rates J. Mol. Biol. 320, 645-661 (Pubitemid 34753986)
4. Wang, L., Erlandsen, H., Haavik, J., Knappskog, P. M., and Stevens, R. C. (2002) Three-dimensional structure of human tryptophan hydroxylase and its implications for the biosynthesis of the neurotransmitters serotonin and melatonin Biochemistry 41, 12569-12574 (Pubitemid 35192485)
5. Goodwill, K. E., Sabatier, C., Marks, C., Raag, R., Fitzpatrick, P. F., and Stevens, R. C. (1997) Crystal structure of tyrosine hydroxylase at 2.3 Å and its implications for inherited neurodegenerative diseases Nat. Struct. Biol. 4, 578-585
6. 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. Inorg. Chem. 10, 87-93 (Pubitemid 40569003)
7. Fitzpatrick, P. F. (2003) Mechanism of aromatic amino acid hydroxylation Biochemistry 42, 14083-14091 (Pubitemid 37499404)
8. Loeb, K. E., Westre, T. E., Kappock, T. J., Mitić, N., Glasfeld, E., Caradonna, J. P., Hedman, B., Hodgson, K. O., and Solomon, E. I. (1997) Spectroscopic characterization of the catalytically competent ferrous site of the resting, activated, and substrate-bound forms of phenylalanine hydroxylase J. Am. Chem. Soc. 119, 1901-1915 (Pubitemid 27148104)
9. Andersen, O. A., Stokka, A. J., Flatmark, T., and Hough, E. (2003) 2.0 Å resolution crystal structures of the ternary complexes of human phenylalanine hydroxylase catalytic domain with tetrahydrobiopterin and 3-(2-thienyl)- l -alanine or l -norleucine: Substrate specificity and molecular motions related to substrate binding J. Mol. Biol. 333, 747-757 (Pubitemid 37268016)
10. 2 activation J. Am. Chem. Soc. 131, 7685-7698
11. Eser, B. E. and Fitzpatrick, P. F. (2010) Measurement of intrinsic rate constants in the tyrosine hydroxylase reaction Biochemistry 49, 645-652
12. 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 (Pubitemid 47555542)
13. Hillas, P. J. and Fitzpatrick, P. F. (1996) A mechanism for hydroxylation by tyrosine hydroxylase based on partitioning of substituted phenylalanines Biochemistry 35, 6969-6975
14. Moran, G. R., Derecskei-Kovacs, A., Hillas, P. J., and Fitzpatrick, P. F. (2000) On the catalytic mechanism of tryptophan hydroxylase J. Am. Chem. Soc. 122, 4535-4541 (Pubitemid 30331666)
15. Frantom, P. A. and Fitzpatrick, P. F. (2003) Uncoupled forms of tyrosine hydroxylase unmask kinetic isotope effects on chemical steps J. Am. Chem. Soc. 125, 16190-16191 (Pubitemid 38020636)
16. Pavon, J. A. and Fitzpatrick, P. F. (2006) Insights into the catalytic mechanisms of phenylalanine and tryptophan hydroxylase from kinetic isotope effects on aromatic hydroxylation Biochemistry 45, 11030-11037 (Pubitemid 44360174)
17. Panay, A. J. and Fitzpatrick, P. F. (2008) Kinetic isotope effects on aromatic and benzylic hydroxylation by Chromobacterium violaceum phenylalanine hydroxylase as probes of chemical mechanism and reactivity Biochemistry 47, 11118-11124
18. Pavon, J. A. and Fitzpatrick, P. F. (2005) Intrinsic isotope effects on benzylic hydroxylation by the aromatic amino acid hydroxylases: Evidence for hydrogen tunneling, coupled motion, and similar reactivities J. Am. Chem. Soc. 127, 16414-16415 (Pubitemid 41740390)
19. Panay, A. J. and Fitzpatrick, P. F. (2010) Measurement of the intramolecular isotope effect on aliphatic hydroxylation by Chromobacterium violaceum phenylalanine hydroxylase J. Am. Chem. Soc. 132, 5584-5585
20. Proshlyakov, D. A., Henshaw, T. F., Moterosso, G. R., Ryle, M. J., and Hausinger, R. P. (2004) Direct detection of oxygen intermediates in the non-heme Fe enzyme taurine/α-ketoglutarate dioxygenase J. Am. Chem. Soc. 126, 1022-1023 (Pubitemid 38140723)
21. 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 Fe(IV) complex in taurine/α-ketoglutarate dioxygenase (TauD) from Escherichia coli Biochemistry 42, 7497-7508 (Pubitemid 36740493)
22. Riggs-Gelasco, P. J., Price, J. C., Guyer, R. B., Brehm, J. H., Barr, E. W., Bollinger, J. M., Jr., and Krebs, C. (2004) EXAFS spectroscopic evidence for an Fe=O unit in the Fe(IV) intermediate observed during oxygen activation by taurine:α-ketoglutarate dioxygenase J. Am. Chem. Soc. 126, 8108-8109 (Pubitemid 38878945)
23. Krebs, C., Price, J. C., Baldwin, J., Saleh, L., Green, M. T., and Bollinger, J. M., Jr. (2005) Rapid freeze-quench Mössbauer spectroscopy: Monitoring changes of an iron-containing site during a biochemical reaction Inorg. Chem. 44, 742-757 (Pubitemid 40255945)
24. Bollinger, J. M., Jr., Price, J. C., Hoffart, L. M., Barr, E. W., and Krebs, C. (2005) Mechanism of taurine:α-ketoglutarate dioxygenase (TauD) from Escherichia coli Eur. J. Inorg. Chem. 2005, 4245-4254 (Pubitemid 41587542)
25. Pavon, J. A. and Fitzpatrick, P. F. (2009) Demonstration of a peroxide shunt in the tetrahydropterin-dependent aromatic amino acid monooxygenases J. Am. Chem. Soc. 131, 4582-4583
26. Baldwin, J., Krebs, C., Ley, B. A., Edmondson, D. E., Huynh, B. H., and Bollinger, J. M., Jr. (2000) Mechanism of rapid electron transfer during oxygen activation in the R2 subunit of Escherichia coli ribonucleotide reductase. 1. Evidence for a transient tryptophan radical J. Am. Chem. Soc. 122, 12195-12206 (Pubitemid 32062257)
27. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global Kinetic Explorer: A new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387, 20-29
28. 57Fe Mossbauer spectroscopy. In Physical Methods in Bioinorganic Chemistry (Que, L., Jr., Ed.) pp 287 - 319, University Science Books, Sausalito, CA.
29. 2+ complexes in their lowest triplet and quintet states using multireference ab initio and density functional theory methods J. Inorg. Biochem. 100, 716-726
30. Hoffart, L. M., Barr, E. W., Guyer, R. B., Bollinger, J. M., Jr., and Krebs, C. (2006) Direct spectroscopic detection of a C-H-cleaving high-spin Fe(IV) complex in a prolyl-4-hydroxylase Proc. Natl. Acad. Sci. U.S.A. 103, 14738-14743 (Pubitemid 44529674)
31. Price, J. C., Barr, E. W., Glass, T. E., Krebs, C., and Bollinger, J. M., Jr. (2003) Evidence for hydrogen abstraction from C1 of taurine by the high-spin Fe(IV) intermediate detected during oxygen activation by taurine:α-ketoglutarate dioxygenase (TauD) J. Am. Chem. Soc. 125, 13008-13009 (Pubitemid 37305581)
32. Bollinger, J. M., Jr. and Krebs, C. (2006) Stalking intermediates in oxygen activation by iron enzymes: Motivation and method J. Inorg. Biochem. 100, 586-605
33. Carr, R. T., Balasubramanian, S., Hawkins, P. C. D., and Benkovic, S. J. (1995) Mechanism of metal-independent hydroxylation by Chromobacterium violaceum phenylalanine hydroxylase Biochemistry 34, 7525-7532
34. Panay, A. J. (2010) Mechanistic, Structural and Functional Studies on Phenylalanine Hydroxylase from Chromobacterium violaceum. Ph.D. Dissertation, Texas A&M University, College Station, TX.
35. Matthews, M. L., Krest, C. M., Barr, E. W., Vaillancourt, F. H., Walsh, C. T., Green, M. T., Krebs, C., and Bollinger, J. M., Jr. (2009) Substrate-triggered formation and remarkable stability of the C-H bond-cleaving chloroferryl intermediate in the aliphatic halogenase, SyrB2 Biochemistry 48, 4331-4343
36. Pember, S. O., Johnson, K. A., Villafranca, J. J., and Benkovic, S. J. (1989) Mechanistic studies on phenylalanine hydroxylase from Chromobacterium violaceum. Evidence for the formation of an enzyme-oxygen complex Biochemistry 28, 2124-2130
37. Volner, A., Zoidakis, J., and Abu-Omar, M. M. (2003) Order of substrate binding in bacterial phenylalanine hydroxylase and its mechanistic implication for pterin-dependent oxygenases J. Biol. Inorg. Chem. 8, 121-128 (Pubitemid 36172455)
38. Galonić, D. P., Barr, E. W., Walsh, C. T., Bollinger, J. M., Jr., and Krebs, C. (2007) Two interconverting Fe(IV) intermediates in aliphatic chlorination by the halogenase CytC3 Nat. Chem. Biol. 3, 113-116 (Pubitemid 46134998)
39. Galonić Fujimori, D., Barr, E. W., Matthews, M. L., Koch, G. M., Yonce, J. R., Walsh, C. T., Bollinger, J. M., Jr., Krebs, C., and Riggs-Gelasco, P. J. (2007) Spectroscopic evidence for a high-spin Br-Fe(IV)-oxo intermediate in the α-ketoglutarate-dependent halogenase CytC3 from Streptomyces J. Am. Chem. Soc. 129, 13408-13409 (Pubitemid 350071767)
40. Sinnecker, S., Svensen, N., Barr, E. W., Ye, S., Bollinger, J. M., Jr., Neese, F., and Krebs, C. (2007) Spectroscopic and computational evaluation of the structure of the high-spin Fe(IV)-oxo intermediates in taurine:α- ketoglutarate dioxygenase from Escherichia coli and its His99Ala ligand variant J. Am. Chem. Soc. 129, 6168-6179 (Pubitemid 46786807)
41. Andersen, O. A., Flatmark, T., and Hough, E. (2001) High resolution crystal structures of the catalytic domain of human phenylalanine hydroxylase in its catalytically active Fe(II) form and binary complex with tetrahydrobiopterin J. Mol. Biol. 314, 279-291 (Pubitemid 33105093)
42. Leiros, H.-K. S., Pey, A. L., Innselset, M., Moe, E., Leiros, I., Steen, I. H., and Martinez, A. (2007) Structure of phenylalanine hydroxylase from Colwellia psychrerythraea 34H, a monomeric cold active enzyme with local flexibility around the active site and high overall stability J. Biol. Chem. 282, 21973-21986 (Pubitemid 47195741)
43. Wasinger, E. C., Mitić, N., Hedman, B., Caradonna, J., Solomon, E. I., and Hodgson, K. O. (2002) X-ray absorption spectroscopic investigation of the resting ferrous and cosubstrate-bound active sites of phenylalanine hydroxylase Biochemistry 41, 6211-6217 (Pubitemid 34525984)
44. Andersen, O. A., Flatmark, T., and Hough, E. (2002) Crystal structure of the ternary complex of the catalytic domain of human phenylalanine hydroxylase with tetrahydrobiopterin and 3-(2-thienyl)- l -alanine, and its implications for the mechanism of catalysis and substrate activation J. Mol. Biol. 320, 1095-1108 (Pubitemid 34808826)
45. Fierke, C. A., Hammes, G. G., and Daniel, L. P. (1995) Transient kinetic approaches to enzyme mechanisms Methods Enzymol. 249, 3-37
46. Pavon, J. A., Eser, B. E., Huynh, M. T., and Fitzpatrick, P. F. (2010) Single turnover kinetics of tryptophan hydroxylase: Evidence for a new intermediate in the reaction of the aromatic amino acid hydroxylases Biochemistry 49, 7563-7571