What's new in enzymatic halogenations

Current Opinion in Chemical Biology

Volumn 11, Issue 5, 2007, Pages 553-560

  Fujimori, Danica Galonić ^a   Walsh, Christopher T ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HALIDE; HALOGEN; HALOPEROXIDASE; HYDROGEN PEROXIDE; NATURAL PRODUCT; PEROXIDASE; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG;

BIOINFORMATICS; ELECTRON TRANSPORT; ENZYME ACTIVITY; GENE SEQUENCE; GENOME; HALOGENATION; ORGANIC CHEMISTRY; OXIDATION; OXIDATION REDUCTION REACTION; REACTION ANALYSIS; REVIEW; SEQUENCE ANALYSIS;

BIOLOGICAL PRODUCTS; HALOGENATION; OXIDATION-REDUCTION; PEROXIDASES;

EID: 35348834136     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2007.08.002     Document Type: Review

References (67)

1. Vaillancourt F.H., Yeh E., Vosburg D.A., Garneau-Tsodikova S., and Walsh C.T. Nature's inventory of halogenation catalysts: oxidative strategies predominate. Chem Rev 106 (2006) 3364-3378. The review provides a comprehensive insight into the biological halogenation catalysts.
2. Morrison M., and Schonbaum G.R. Peroxidase-catalyzed halogenation. Annu Rev Biochem 45 (1976) 861-888
3. van Pee K.H. Biosynthesis of halogenated metabolites by bacteria. Annu Rev Microbiol 50 (1996) 375-399
4. Piraee M., White R.L., and Vining L.C. Biosynthesis of the dichloroacetyl component of chloramphenicol in Streptomyces venezuelae ISP5230: genes required for halogenation. Microbiology 150 (2004) 85-94
5. Kahne D., Leimkuhler C., Lu W., and Walsh C. Glycopeptide and lipoglycopeptide antibiotics. Chem Rev 105 (2005) 425-448
6. Harris C., Kannan R., Kopecka H., and Harris T. The role of chlorine substituents in the antibiotic vancomycin: preparation and characterization of mono- and didechlorovancomycin. J Am Chem Soc 107 (1985) 6652-6658
7. Kay R.R. The biosynthesis of differentiation-inducing factor, a chlorinated signal molecule regulating Dictyostelium development. J Biol Chem 273 (1998) 2669-2675
8. Gribble G.W. Natural organohalogens-occurrence, sources, quantities, natural function, and benefits. Euro Chlor Science Dossier (2004) 1-77
9. Dairi T., Nakano T., Mizukami T., Aisaka K., Hasegawa M., and Katsumata R. Conserved organization of genes for biosynthesis of chlortetracycline in Streptomyces strains. Biosci Biotechnol Biochem 59 (1995) 1360-1361
10. Hammer P.E., Hill D.S., Lam S.T., Van Pee K.H., and Ligon J.M. Four genes from Pseudomonas fluorescens that encode the biosynthesis of pyrrolnitrin. Appl Environ Microbiol 63 (1997) 2147-2154
11. Pelzer S., Sussmuth R., Heckmann D., Recktenwald J., Huber P., Jung G., and Wohlleben W. Identification and analysis of the balhimycin biosynthetic gene cluster and its use for manipulating glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908. Antimicrob Agents Chemother 43 (1999) 1565-1573
12. van Wageningen A.M., Kirkpatrick P.N., Williams D.H., Harris B.R., Kershaw J.K., Lennard N.J., Jones M., Jones S.J., and Solenberg P.J. Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic. Chem Biol 5 (1998) 155-162
13. Nowak-Thompson B., Chaney N., Wing J.S., Gould S.J., and Loper J.E. Characterization of the pyoluteorin biosynthetic gene cluster of Pseudomonas fluorescens Pf-5. J Bacteriol 181 (1999) 2166-2174
14. Zhang J.H., Quigley N.B., and Gross D.C. Analysis of the syrB and syrC genes of Pseudomonas syringae pv. syringae indicates that syringomycin is synthesized by a thiotemplate mechanism. J Bacteriol 177 (1995) 4009-4020
15. Guenzi E., Galli G., Grgurina I., Gross D.C., and Grandi G. Characterization of the syringomycin synthetase gene cluster. A link between prokaryotic and eukaryotic peptide synthetases. J Biol Chem 273 (1998) 32857-32863
16. Chang Z., Sitachitta N., Rossi J.V., Roberts M.A., Flatt P.M., Jia J., Sherman D.H., and Gerwick W.H. Biosynthetic pathway and gene cluster analysis of curacin A, an antitubulin natural product from the tropical marine cyanobacterium Lyngbya majuscula. J Nat Prod 67 (2004) 1356-1367
17. Chang Z., Flatt P., Gerwick W.H., Nguyen V.A., Willis C.L., and Sherman D.H. The barbamide biosynthetic gene cluster: a novel marine cyanobacterial system of mixed polyketide synthase (PKS)-non-ribosomal peptide synthetase (NRPS) origin involving an unusual trichloroleucyl starter unit. Gene 296 (2002) 235-247
18. Buell C.R., Joardar V., Lindeberg M., Selengut J., Paulsen I.T., Gwinn M.L., Dodson R.J., Deboy R.T., Durkin A.S., Kolonay J.F., et al. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 100 (2003) 10181-10186
19. Ullrich M., Guenzi A.C., Mitchell R.E., and Bender C.L. Cloning and expression of genes required for coronamic acid (2-ethyl-1-aminocyclopropane 1-carboxylic acid), an intermediate in the biosynthesis of the phytotoxin coronatine. Appl Environ Microbiol 60 (1994) 2890-2897
20. Edwards D.J., Marquez B.L., Nogle L.M., McPhail K., Goeger D.E., Roberts M.A., and Gerwick W.H. Structure and biosynthesis of the jamaicamides, new mixed polyketide-peptide neurotoxins from the marine cyanobacterium Lyngbya majuscula. Chem Biol 11 (2004) 817-833
21. Ueki M., Galonić D.P., Vaillancourt F.H., Garneau-Tsodikova S., Yeh E., Vosburg D.A., Schroeder F.C., Osada H., and Walsh C.T. Enzymatic generation of the antimetabolite γ, γ-dichloroaminobutyrate by NRPS and mononuclear iron halogenase action in a streptomycete. Chem Biol 13 (2006) 1183-1191
22. Keller S., Wage T., Hohaus K., Holzer M., Eichhorn E., and van Pee K.H. Purification and partial characterization of tryptophan 7-halogenase (PrnA) from Pseudomonas fluorescens. Angew Chem Int Ed Engl 39 (2000) 2300-2302
23. 2-dependent halogenase. Proc Natl Acad Sci U S A 102 (2005) 10111-10116. SyrB2 is the first in vitro reconstituted mononuclear nonheme iron halogenase. Herein cofactor requirements of this enzyme are described in detail.
24. Yeh E., Blasiak L.C., Koglin A., Drennan C.L., and Walsh C.T. Chlorination by a long-lived intermediate in the mechanism of flavin-dependent halogenases. Biochemistry 46 (2007) 1284-1292. Characterization of a kinetically competent, long-lived intermediate in flavin-dependent halogenase RebH is described. It is postulated that this intermediate is the chloramine species obtained in the reaction of HOCl with an active site lysine residue.
25. Yeh E., Cole L.J., Barr E.W., Bollinger Jr. J.M., Ballou D.P., and Walsh C.T. Flavin redox chemistry precedes substrate chlorination during the reaction of the flavin-dependent halogenase RebH. Biochemistry 45 (2006) 7904-7912. Authors have carried out kinetic characterization of RebH-catalyzed chlorination.
26. Blasiak L.C., Vaillancourt F.H., Walsh C.T., and Drennan C.L. Crystal structure of the non-haem iron halogenase SyrB2 in syringomycin biosynthesis. Nature 440 (2006) 368-371. The crystal structure of nonheme iron halogenase SyrB2 revealed that the active site iron in Fe(II) state is coordinated by two protein-derived histidine residues and a chlorine atom, thus distinguishing halogenases from related dioxygenases.
27. Dong C., Flecks S., Unversucht S., Haupt C., van Pee K.H., and Naismith J.H. Tryptophan 7-halogenase (PrnA) structure suggests a mechanism for regioselective chlorination. Science 309 (2005) 2216-2219. Crystal structure of flavin halogenase PrnA lead to the hypothesis that HOCl is generated during the flavin halogenases catalysis.
28. Galonic D.P., Barr E.W., Walsh C.T., Bollinger Jr. J.M., and Krebs C. Two interconverting Fe(IV) intermediates in aliphatic chlorination by the halogenase CytC3. Nat Chem Biol 3 (2007) 113-116. Stopped-flow absorption and Mössbauer spectroscopies were used to elucidate mechanism of aliphatic halogenation by mononuclear nonheme iron halogenase CytC3. The presence of two interconverting Fe(IV)-oxo intermediates distinguishes aliphatic halogenases from mononuclear nonheme iron dioxygenases.
29. Perrin C.L., Rodgers B.L., and O'Connor J.M. Nucleophilic addition to a p-benzyne derived from an enediyne: a new mechanism for halide incorporation into biomolecules. J Am Chem Soc 129 (2007) 4795-4799. The authors describe a model study of non-enzymatic non-oxidative halogenation of p-benzyne biradical intermediate in Bergman cyclization of an enediyne. This mode of halogenation is postulated to account for the formation of several monochlorinated marine macrolides.
30. Gribble G.W. Natural organohalogens: a new frontier for medicinal agents?. J Chem Ed 81 (2004) 1441-1449
31. van Pee K.H. Microbial biosynthesis of halometabolites. Arch Microbiol 175 (2001) 250-258
32. Butler A., and Walker J.V. Marine haloperoxidases. Chem Rev 93 (1993) 1937-1944
33. Carter-Franklin J.N., and Butler A. Vanadium bromoperoxidase-catalyzed biosynthesis of halogenated marine natural products. J Am Chem Soc 126 (2004) 15060-15066
34. Orjala J., and Gerwick W.H. Barbamide, a chlorinated metabolite with molluscicidal activity from the Caribbean cyanobacterium Lyngbya majuscula. J Nat Prod 59 (1996) 427-430
35. Blunt J.W., Copp B.R., Hu W.P., Munro M.H., Northcote P.T., and Prinsep M.R. Marine natural products. Nat Prod Rep 24 (2007) 31-86
36. Gribble G.W. Naturally occurring organohalogen compounds. Acc Chem Res 31 (1998) 141-152
37. Williamson R.T., Pal Singh I., and Gerwick W.H. Taveuniamides: new chlorinated toxins from a mixed assemblage of marine cyanobacteria. Tetrahedron 60 (2004) 7025-7033
38. Hager L.P., Morris D.R., Brown F.S., and Eberwein H. Chloroperoxidase. II. Utilization of halogen anions. J Biol Chem 241 (1966) 1769-1777
39. van Pee K.H., and Patallo E.P. Flavin-dependent halogenases involved in secondary metabolism in bacteria. Appl Microbiol Biotechnol 70 (2006) 631-641
40. O'Hagan D., Schaffrath C., Cobb S.L., Hamilton J.T., and Murphy C.D. Biochemistry: biosynthesis of an organofluorine molecule. Nature 416 (2002) 279
41. Dong C., Huang F., Deng H., Schaffrath C., Spencer J.B., O'Hagan D., and Naismith J.H. Crystal structure and mechanism of a bacterial fluorinating enzyme. Nature 427 (2004) 561-565
42. Deng H., Cobb S.L., McEwan A.R., McGlinchey R.P., Naismith J.H., O'Hagan D., Robinson D.A., and Spencer J.B. The fluorinase from Streptomyces cattleya is also a chlorinase. Angew Chem Int Ed Engl 45 (2006) 759-762
43. Buchanan G.O., Williams P.G., Feling R.H., Kauffman C.A., Jensen P.R., and Fenical W. Sporolides A and B: structurally unprecedented halogenated macrolides from the marine actinomycete Salinispora tropica. Org Lett 7 (2005) 2731-2734
44. Oh D.C., Williams P.G., Kauffman C.A., Jensen P.R., and Fenical W. Cyanosporasides A and B, chloro- and cyano-cyclopenta[a]indene glycosides from the marine actinomycete 'Salinispora pacifica'. Org Lett 8 (2006) 1021-1024
45. Fenical W., and Jensen P.R. Developing a new resource for drug discovery: marine actinomycete bacteria. Nat Chem Biol 2 (2006) 666-673
46. Udwary D.W., Zeigler L., Asolkar R.N., Singan V., Lapidus A., Fenical W., Jensen P.R., and Moore B.S. Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proc Natl Acad Sci U S A 104 (2007) 10376-10381. Genome sequencing of marine actinomycete Salinispora tropica provides an insight into biosynthesis of a number of secondary metabolites, including anticancer agent salinosporamide A and enediyne-derived chlorinated compounds sporolides A and B.
47. Beckwith J.R., Clark R., and Hager L.P. Biological chlorination. VII. Studies on the biosynthesis of caldariomycin. J Biol Chem 238 (1963) 3086-3090
48. Wagenknecht H.A., and Woggon W.D. Identification of intermediates in the catalytic cycle of chloroperoxidase. Chem Biol 4 (1997) 367-372
49. Soedjak H.S., Walker J.V., and Butler A. Inhibition and inactivation of vanadium bromoperoxidase by the substrate hydrogen peroxide and further mechanistic studies. Biochemistry 34 (1995) 12689-12696
50. Butler A., and Carter-Franklin J.N. The role of vanadium bromoperoxidase in the biosynthesis of halogenated marine natural products. Nat Prod Rep 21 (2004) 180-188
51. Gribble G.W. Naturally occurring halogenated pyrroles and indoles. Prog Heterocycl Chem 15 (2003) 58-74
52. Ishihara J., Shimada Y., Kanoh N., Takasugi Y., Fukuzawa A., and Murai A. Conversion of prelaureatin into laurallene, a bromo-allene compound, by enzymatic and chemical bromo-etherification reactions. Tetrahedron 53 (1997) 8371-8382
53. Naismith J.H. Inferring the chemical mechanism from structures of enzymes. Chem Soc Rev 35 (2006) 763-770
54. Yeh E., Garneau S., and Walsh C.T. 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 (2005) 3960-3965
55. Zehner S., Kotzsch A., Bister B., Sussmuth R.D., Mendez C., Salas J.A., and van Pee K.H. A regioselective tryptophan 5-halogenase is involved in pyrroindomycin biosynthesis in Streptomyces rugosporus LL-42D005. Chem Biol 12 (2005) 445-452
56. Hohaus K., Altmann A., Burd W., Fischer I., Hammer P.E., Hill D.S., Ligon J.M., and van Pee K.-H. NADH-dependent halogenases are more likely to be involved in halometabolite biosynthesis than haloperoxidases. Angew Chem Int Ed Engl 36 (1997) 2012-2013
57. Kling E., Schmid C., Unversucht S., Wage T., Zehner S., and van Pee K.-H. In: Wohlleben W., Spellig T., and Muller-Tiemann B. (Eds). Enzymatic Incorporation of Halogen Atoms into Natural Compounds (2005), Berlin Heidelberg New York, Springer
58. 2-dependent halogenase PltA during pyoluteorin biosynthesis. Proc Natl Acad Sci U S A 102 (2005) 13843-13848
59. Hornung A., Bertazzo M., Dziarnowski A., Schneider K., Welzel K., Wohlert S.E., Holzenkampfer M., Nicholson G.J., Bechthold A., Sussmuth R.D., et al. A genomic screening approach to the structure guided identification of drug candidates from natural sources. Chembiochem 8 (2007) 757-766. Genome-guided discovery of novel halogenated natural products by screening of a large strain collection with primers targeting flavin halogenases is described.
60. Vaillancourt F.H., Yeh E., Vosburg D.A., O'Connor S.E., and Walsh C.T. Cryptic chlorination by a non-haem iron enzyme during cyclopropyl amino acid biosynthesis. Nature 436 (2005) 1191-1194
61. Galonić D.P., Vaillancourt F.H., and Walsh C.T. Halogenation of unactivated carbon centers in natural product biosynthesis: trichlorination of leucine during barbamide biosynthesis. J Am Chem Soc 128 (2006) 3900-3901
62. Costas M., Mehn M.P., Jensen M.P., and Que Jr. L. Dioxygen activation at mononuclear nonheme iron active sites: enzymes, models, and intermediates. Chem Rev 104 (2004) 939-986
63. Price J.C., Barr E.W., Tirupati B., Bollinger Jr. J.M., and Krebs C. 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 (2003) 7497-7508
64. Calderone C.T., Kowtoniuk W.E., Kelleher N.L., Walsh C.T., and Dorrestein P.C. Convergence of isoprene and polyketide biosynthetic machinery: isoprenyl-S-carrier proteins in the pksX pathway of Bacillus subtilis. Proc Natl Acad Sci U S A 103 (2006) 8977-8982
65. Butcher R.A., Schroeder F.C., Fischbach M.A., Straight P.D., Kolter R., Walsh C.T., and Clardy J. The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. Proc Natl Acad Sci U S A 104 (2007) 1506-1509
66. Gu L., Jia J., Liu H., Hakansson K., Gerwick W.H., and Sherman D.H. Metabolic coupling of dehydration and decarboxylation in the curacin a pathway: functional identification of a mechanistically diverse enzyme pair. J Am Chem Soc 128 (2006) 9014-9015
67. Simunovic V., Zapp J., Rachid S., Krug D., Meiser P., and Muller R. Myxovirescin A biosynthesis is directed by hybrid polyketide synthases/nonribosomal peptide synthetase, 3-hydroxy-3-methylglutaryl-CoA synthases, and trans-acting acyltransferases. Chembiochem 7 (2006) 1206-1220