Chlorination by a long-lived intermediate in the mechanism of flavin-dependent halogenases

Biochemistry

Volumn 46, Issue 5, 2007, Pages 1284-1292

  Yeh, Ellen ^a   Blasiak, Leah C ^b   Koglin, Alexander ^a   Drennan, Catherine L ^b   Walsh, Christopher T ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HALOGENASE; OXIDANTS; REBECCAMYCIN; TRYPTOPHANS;

ANTIBODIES; BIOSYNTHESIS; CATALYSIS; CHLORINATION; REACTION KINETICS; SUBSTRATES;

ENZYME KINETICS;

7 CHLOROTRYPTOPHAN; FLAVINE ADENINE NUCLEOTIDE; HYPOCHLORITE; LYSINE; OXIDOREDUCTASE; OXYGEN; PROTEIN REBH; REBECCAMYCIN; TOSYLCHLORAMIDE SODIUM; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CATALYSIS; CHEMICAL REACTION KINETICS; CHLORINATION; ENZYME ACTIVE SITE; ENZYME MECHANISM; HALF LIFE TIME; PRIORITY JOURNAL; STEREOSPECIFICITY;

BINDING SITES; CHLORINE; CRYSTALLOGRAPHY, X-RAY; FLAVIN-ADENINE DINUCLEOTIDE; HYPOCHLOROUS ACID; KINETICS; LYSINE; OXIDOREDUCTASES; OXYGEN; TRYPTOPHAN;

EID: 33846842522     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0621213     Document Type: Article

References (39)

1. Dong, C., Flecks, S., Unversucht, S., Haupt, C., van Pee, K. H., and Naismith, J. H. (2005) Tryptophan 7-halogenase (PrnA) structure suggests a mechanism for regioselective chlorination, Science 309, 2216-2219.
2. Yeh, E., Cole, L. J., Barr, E. W., Bollinger, J. M., Ballou, D. P., and Walsh, C. T. (2006) Flavin redox chemistry precedes substrate chlorination in the reaction of the flavin-dependent halogenase RebH, Biochemistry 45, 7904-7912.
3. Keller, S., Wage, T., Hohaus, K., Holzer, M., Eichhorn, E., and van Pee, K. H. (2000) Purification and partial characterization of tryptophan 7-halogenase (PrnA) from Pseudomonas fluorescens, Angew. Chem., Int. Ed. 39, 2300-2302.
4. Yeh, E., Garneau, S., and Walsh, C. T. (2005) Robust in vitro activity of RebF and RebH, a two-component reductase/halogenase, generating 7-chlorotryptophan during rebeccamycin biosynthesis, Proc. Natl. Acad. Sci. U.S.A. 102, 3960-3965.
5. Hazen, S. L., Hsu, F. F., d'Avignon, A., and Heinecke, J. W. (1998) Human neutrophils employ myeloperoxidase to convert alpha-amino acids to a battery of reactive aldehydes: a pathway for aldehyde generation at sites of inflammation, Biochemistry 37, 6864-6873.
6. Nightingale, Z. D., Lancha, A. H., Jr., Handelman, S. K., Dolnikowski, G. G., Busse, S. C., Dratz, E. A., Blumberg, J. B., and Handelman, G. J. (2000) Relative reactivity of lysine and other peptide-bound amino acids to oxidation by hypochlorite, Free Radical Biol. Med. 29, 425-433.
7. Peskin, A. V., and Winterbourn, C. C. (2001) Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate, Free Radical Biol. Med. 30, 572-579.
8. Pattison, D. I., and Davies, M. J. (2001) Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds, Chem. Res. Toxicol. 14, 1453-1464.
9. Hawkins, C. L., Pattison, D. I., and Davies, M. J. (2003) Hypochlorite-induced oxidation of amino acids, peptides and proteins, Amino Acids 25, 259-274.
10. Vaillancourt, F. H., Yeh, E., Vosburg, D. A., Garneau-Tsodikova, S., and Walsh, C. T. (2006) Nature's inventory of halogenation catalysts: Oxidative strategies predominate, Chem. Rev. 106, 3364-3378.
11. Naismith, J. H. (2006) Inferring the chemical mechanism from structures of enzymes, Chem. Soc. Rev. 35, 763-770.
12. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
13. Collaborative Computational Project, No. 4 (1994) The CCP4 suite: Programs for protein crystallography, Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763.
14. Read, R. J. (2001) Pushing the boundaries of molecular replacement with maximum likelihood, Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 1373-1382.
15. McRee, D. E. (1999) XtalView/Xfit - A versatile program for manipulating atomic coordinates and electron density, J. Struct. Biol. 125, 156-165.
16. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics, Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132.
17. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., PAnnu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921.
18. Kleywegt, G. J., and Jones, T. A. (1998) Databases in protein crystallography, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 1119-1131.
19. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK - a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
20. Delano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA.
21. Dorrestein, P. C., Yeh, E., Garneau-Tsodikova, S., Kelleher, N. L., and Walsh, C. T. (2005) Dichlorination of a pyrrolyl-S-carrier protein by FADH2-dependent halogenase PltA during pyoluteorin biosynthesis, Proc. Natl. Acad. Sci. U.S.A. 102, 13843-13848.
22. Thomas, E. L., Grisham, M. B., and Jefferson, M. M. (1986) Preparation and characterization of chloramines, Methods Enzymol. 132, 569-585.
23. Weiss, S. J., Lampert, M. B., and Test, S. T. (1983) Long-lived oxidants generated by human neutrophils: characterization and bioactivity, Science 222, 625-628.
24. Test, S. T., Lampert, M. B., Ossanna, P. J., Thoene, J. G., and Weiss, S. J. (1984) Generation of nitrogen-chlorine oxidants by human phagocytes, J. Clin. Invest. 74, 1341-1349.
25. Domigan, N. M., Charlton, T. S., Duncan, M. W., Winterbourn, C. C., and Kettle, A. J. (1995) Chlorination of tyrosyl residues in peptides by myeloperoxidase and human neutrophils, J. Biol. Chem. 270, 16542-16548.
26. Bergt, C., Fu, X., Huq, N. P., Kao, J., and Heinecke, J. W. (2004) Lysine residues direct the chlorination of tyrosines in YXXK motifs of apolipoprotein A-I when hypochlorous acid oxidizes high density lipoprotein, J. Biol. Chem. 279, 7856-7866.
27. Pattison, D. I., and Davies, M. J. (2005) Kinetic analysis of the role of histidine chloramines in hypochlorous acid mediated protein oxidation, Biochemistry 44, 7378-7387.
28. Rudie, N. G., Porter, D. J., and Bright, H. J. (1980) Chlorination of an active site tyrosyl residue in D-amino acid oxidase by N-chloro-D-leucine, J. Biol. Chem. 255, 498-508.
29. Ronchi, S., Galliano, M., Minchiotti, L., Curti, B., Rudie, N. G., Porter, D. J., and Bright, H. J. (1980) An active site-tyrosine-containing heptapeptide from D-amino acid oxidase, J. Biol. Chem 255, 6044-6046.
30. Weil, I., and Morris, J. C. (1949) Equilibrium studies on N-chloro compounds, J. Am. Chem. Soc. 71.
31. Gray, E. T., Jr., Margerum, D. W., and Huffman, R. P. (1978) Chloramine equilibria and the kinetics of disproportionation in aqueous solution, ACS Symp. Ser. 82, 264-277.
32. Snyder, M. P., and Margerum, D. W. (1982) Kinetics of chlorine transfer from chloramines to amines, amino acids, and peptides, Inorg. Chem. 21, 2545-2550.
33. Zehner, S., Kotzsch, A., Bister, B., Sussmuth, R. D., Mendez, C, Salas, J. A., and van Pee, K. H. (2005) A regioselective tryptophan 5-halogenase is involved in pyrroindomycin biosynthesis in Streptomyces rugosporus LL-42D005, Chem. Biol. 12, 445-452.
34. van Pee, K. H. (2001) Microbial biosynthesis of halometabolites, Arch. Microbiol. 175, 250-258.
35. Geigert, J., Neidleman, S. L., and Dalietos, D. J. (1983) Novel haloperoxidase substrates. Alkynes and cyclopropanes, J. Biol. Chem. 258, 2273-2277.
36. 2 as enzyme-generated intermediates in chloroperoxidase-catalyzed reactions, J. Biol. Chem. 267, 1769-1775.
37. 2 by the formation of peracetic acid, Angew. Chem., Int. Ed. 36, 1196-1199.
38. Kirk, O., and Conrad, L. S. (1999) Metal-free haloperoxidases: Fact or artifact?, Angew. Chem., Int. Ed. 38, 977-979.
39. Puk, O., Huber, P., Bischoff, D., Recktenwald, J., Jung, G., Sussmuth, R. D., van Pee, K. H., Wohlleben, W., and Pelzer, S. (2002) Glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908: Function of a halogenase and a haloperoxidase/perhydrolase, Chem. Biol. 9, 225-235.