Scope and potential of halogenases in biosynthetic applications

Current Opinion in Chemical Biology

Volumn 17, Issue 2, 2013, Pages 276-283

  Smith, Duncan R M ^a   Grüschow, Sabine ^a   Goss, Rebecca JM ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALIPHATIC COMPOUND; AROMATIC COMPOUND; CHLORAMPHENICOL; CURACIN A; HALOPEROXIDASE; OXIDOREDUCTASE; PRNA PROTEIN; RADICICOL; REBECCAMYCIN; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG;

ASCOPHYLLUM; ELECTRON TRANSPORT; HALOGENATION; REVIEW;

BIOTECHNOLOGY; HALOGENS; HYDROCARBONS, HALOGENATED; OXIDOREDUCTASES; SYNTHETIC BIOLOGY;

EID: 84876741871     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2013.01.018     Document Type: Review

References (58)

1. Gribble G.W. Naturally Occurring Organohalogen Compounds-A Comprehensive Update 2010, vol 91. Springer, Wien.
2. Laus G. Biological activities of natural halogen compounds. Studies in Natural Products Chemistry. Part F 2001, vol 25:757-809. Elsevier Science & Technology.
3. Gu L.C., Wang B., Kulkarni A., Geders T.W., Grindberg R.V., Gerwick L., Håkansson K., Wipf P., Smith J.L., Gerwick W.H., Sherman D.H. Metamorphic enzyme assembly in polyketide diversification. Nature 2009, 459:731-735.
4. Murphy C.D. New frontiers in biological halogenation. J Appl Microbiol 2003, 94:539-548.
5. Roy A.D., Grüschow S., Cairns N., Goss R.J.M. Gene expression enabling synthetic diversification of natural products: chemogenetic generation of pacidamycin analogs. J Am Chem Soc 2010, 132:12243-12245.
6. Müller K., Faeh C., Diederich F. Fluorine in pharmaceuticals: looking beyond intuition. Science 2007, 317:1881-1886.
7. Fujimori D.G., Walsh C.T. What's new in enzymatic halogenations. Curr Opin Chem Biol 2007, 11:553-560.
8. Neumann C.S., Fujimori D.G., Walsh C.T. Halogenation strategies in natural product biosynthesis. Chem Biol 2008, 15:99-109.
9. Ruf J., Carayon P. Structural and functional aspects of thyroid peroxidase. Arch Biochem Biophys 2006, 445:269-277.
10. Fujimori D.G., Barr E.W., Matthews M.L., Koch G.M., Yonce J.R., Walsh C.T., Bollinger J.M., Krebs C., Riggs-Gelasco P.J. Spectroscopic evidence for a high-spin Br-Fe(IV)-oxo intermediate in the alpha-ketoglutarate-dependent halogenase CytC3 from Streptomyces. J Am Chem Soc 2007, 129:13408-13409.
11. Collins D.P., Isaac I.S., Coulter E.D., Hager P.W., Ballou D.P., Dawson J.H. Reaction of ferric Caldariomyces fumago chloroperoxidase with meta-chloroperoxybenzoic acid: sequential formation of compound I, compound II and regeneration of the ferric state using one reactant. J Porphyr Phthalocya 2012, (online).
12. 490. J Biol Chem 1999, 274:23820-23827.
13. Wischang D., Hartung J. Parameters for bromination of pyrroles in bromoperoxidase-catalyzed oxidations. Tetrahedron 2011, 67:4048-4054.
14. Zhang J., Roberge C., Reddy J., Connors N., Chartrain M., Buckland B., Greasham R. Bioconversion of indene to trans-2S,1S-bromoindanol and 1S,2R-indene oxide by a bromoperoxidase/dehydrogenase preparation from Curvularia protuberata MF5400. Enzyme Microb Technol 1999, 24:86-95.
15. Winter J.M., Moore B.S. Exploring the chemistry and biology of vanadium-dependent haloperoxidases. J Biol Chem 2009, 284:18577-18581.
16. Bernhardt P., Okino T., Winter J.M., Miyanaga A., Moore B.S. A stereoselective vanadium-dependent chloroperoxidase in bacterial antibiotic biosynthesis. J Am Chem Soc 2011, 133:4268-4270.
17. Kaysser L., Bernhardt P., Nam S.J., Loesgen S., Ruby J.G., Skewes-Cox P., Jensen P.R., Fenical W., Moore B.S. Merochlorins A-D, cyclic meroterpenoid antibiotics biosynthesized in divergent pathways with vanadium-dependent chloroperoxidases. J Am Chem Soc 2012, 134:11988-11991.
18. Keller S., Wage T., Hohaus K., Holzer M., Eichhorn E., van Pée K.H. Purification and partial characterization of tryptophan 7-halogenase (Prna) from Pseudomonas fluorescens. Angew Chem Int Edit 2000, 39:2300-2302.
19. Chen X.P., van Pée K.H. Catalytic mechanisms, basic roles, and biotechnological and environmental significance of halogenating enzymes. Acta Biochim Biophys Sin 2008, 40:183-193.
20. Blasiak L.C., Drennan C.L. Structural perspective on enzymatic halogenation. Accounts Chem Res 2009, 42:147-155.
21. Podzelinska K., Latimer R., Bhattacharya A., Vining L.C., Zechel D.L., Jia Z.C. Chloramphenicol biosynthesis: the structure of CmlS, a flavin-dependent halogenase showing a covalent flavin-aspartate bond. J Mol Biol 2010, 397:316-331.
22. 2-dependent halogenase PltA during pyoluteorin biosynthesis. Proc Natl Acad Sci U S A 2005, 102:13843-13848.
23. Wohlleben W., Stegmann E., Süssmuth R.D. Molecular genetic approaches to analyze glycopeptide biosynthesis. Methods Enzymol 2009, 458:459-486.
24. Jones A.C., Monroe E.A., Eisman E.B., Gerwick L., Sherman D.H., Gerwick W.H. The unique mechanistic transformations involved in the biosynthesis of modular natural products from marine cyanobacteria. Nat Prod Rep 2010, 27:1048-1065.
25. Allard P.M., Martin M.T., Dau M., Leyssen P., Gueritte F., Litaudon M. Trigocherrin A, the first natural chlorinated daphnane diterpene orthoester from Trigonostemon cherrieri. Org Lett 2012, 14:342-345.
26. Akey D.L., Gehret J.J., Khare D., Smith J.L. Insights from the sea: structural biology of marine polyketide synthases. Nat Prod Rep 2012, 29:1038-1049.
27. Krebs C., Fujimori D.G., Walsh C.T., Bollinger J.M. Non-heme Fe(IV)-oxo intermediates. Accounts Chem Res 2007, 40:484-492.
28. Khare D., Wang B., Gu L.C., Razelun J., Sherman D.H., Gerwick W.H., Håkansson K., Smith J.L. Conformational switch triggered by alpha-ketoglutarate in a halogenase of curacin A biosynthesis. Proc Natl Acad Sci U S A 2010, 107:14099-14104.
29. Matthews M.L., Neumann C.S., Miles L.A., Grove T.L., Booker S.J., Krebs C., Walsh C.T., Bollinger J.M. Substrate positioning controls the partition between halogenation and hydroxylation in the aliphatic halogenase, SyrB2. Proc Natl Acad Sci U S A 2009, 106:17723-17728.
30. Galonic D.P., Vaillancourt F.H., Walsh C.T. Halogenation of unactivated carbon centers in natural product biosynthesis: trichlorination of leucine during barbamide biosynthesis. J Am Chem Soc 2006, 128:3900-3901.
31. Flatt P.M., O'Connell S.J., McPhail K.L., Zeller G., Willis C.L., Sherman D.H., Gerwick W.H. Characterization of the initial enzymatic steps of barbamide biosynthesis. J Nat Prod 2006, 69:938-944.
32. 2-dependent halogenase. Proc Natl Acad Sci U S A 2005, 102:10111-10116.
33. O'Hagan D., Schaffrath C., Cobb S.L., Hamilton J.T.G., Murphy C.D. Biosynthesis of an organofluorine molecule-a fluorinase enzyme has been discovered that catalyses carbon-fluorine bond formation. Nature 2002, 416:279.
34. N2 reaction mechanism. Chembiochem 2004, 5:685-690.
35. Dong C.J., Huang F.L., Deng H., Schaffrath C., Spencer J.B., O'Hagan D., Naismith J.H. Crystal structure and mechanism of a bacterial fluorinating enzyme. Nature 2004, 427:561-565.
36. Huang F.L., Haydock S.F., Spiteller D., Mironenko T., Li T.L., O'Hagan D., Leadlay P.F., Spencer J.B. The gene cluster for fluorometabolite biosynthesis in Streptomyces cattleya: a thioesterase confers resistance to fluoroacetyl-coenzyme A. Chem Biol 2006, 13:475-484.
37. Deng H., Cross S.M., McGlinchey R.P., Hamilton J.T.G., O'Hagan D. In vitro reconstituted biotransformation of 4-fluorothreonine from fluoride ion: application of the fluorinase. Chem Biol 2008, 15:1268-1276.
38. Deng H., Cobb S.L., McEwan A.R., McGlinchey R.P., Naismith J.H., O'Hagan D., Robinson D.A., Spencer J.B. The fluorinase from Streptomyces cattleya is also a chlorinase. Angew Chem Int Edit 2006, 45:759-762.
39. Eustáquio A.S., Pojer F., Noel J.P., Moore B.S. Discovery and characterization of a marine bacterial SAM-dependent chlorinase. Nat Chem Biol 2008, 4:69-74.
40. Eustáquio A.S., O'Hagan D., Moore B.S. Engineering fluorometabolite production: fluorinase expression in Salinispora tropica yields fluorosalinosporamide. J Nat Prod 2010, 73:378-382.
41. Schmidberger J.W., James A.B., Edwards R., Naismith J.H., O'Hagan D. Halomethane biosynthesis: structure of a SAM-dependent halide methyltransferase from Arabidopsis thaliana. Angew Chem Int Edit 2010, 49:3646-3648.
42. Williams R.M., Stocking E.M., Sanz-Cervera J.F. Biosynthesis of prenylated alkaloids derived from tryptophan. Biosynth Aromat Polyketides Isoprenoids Alkaloids 2000, 209:97-173.
43. De Luca V., Laflamme P. The expanding universe of alkaloid biosynthesis. Curr Opin Plant Biol 2001, 4:225-233.
44. Li S.M. Prenylated indole derivatives from fungi: structure diversity, biological activities, biosynthesis and chemoenzymatic synthesis. Nat Prod Rep 2010, 27:57-78.
45. Sánchez C., Zhu L.L., Braña A.F., Salas A.P., Rohr J., Méndez C., Salas J.A. Combinatorial biosynthesis of antitumor indolocarbazole compounds. Proc Natl Acad Sci U S A 2005, 102:461-466.
46. Yeh E., Garneau S., 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 2005, 102:3960-3965.
47. Zehner S., Kotzsch A., Bister B., Süssmuth R.D., Méndez C., Salas J.A., van Pée K.H. A regioselective tryptophan 5-halogenase is involved in pyrroindomycin biosynthesis in Streptomyces rugosporus ll-42D005. Chem Biol 2005, 12:445-452.
48. Seibold C., Schnerr H., Rumpf J., Kunzendorf A., Hatscher C., Wage T., Ernyei A.J., Dong C.J., Naismith J.H., van Pée K.H. A flavin-dependent tryptophan 6-halogenase and its use in modification of pyrrolnitrin biosynthesis. Biocatal Biotransform 2006, 24:401-408.
49. Eustáquio A.S., Gust B., Li S.M., Pelzer S., Wohlleben W., Chater K.F., Heide L. Production of 8'-halogenated and 8'-unsubstituted novobiocin derivatives in genetically engineered Streptomyces coelicolor strains. Chem Biol 2004, 11:1561-1572.
50. Heide L., Westrich L., Anderle C., Gust B., Kammerer B., Piel J. Use of a halogenase of hormaomycin biosynthesis for formation of new clorobiocin analogues with 5-chloropyrrole moieties. Chembiochem 2008, 9:1992-1999.
51. Runguphan W., Qu X.D., O'Connor S.E. Integrating carbon-halogen bond formation into medicinal plant metabolism. Nature 2010, 468:461-U294.
52. Glenn W.S., Nims E., O'Connor S.E. Reengineering a tryptophan halogenase to preferentially chlorinate a direct alkaloid precursor. J Am Chem Soc 2011, 133:19346-19349.
53. Lang A., Polnick S., Nicke T., William P., Patallo E.P., Naismith J.H., van Pée K.H. Changing the regioselectivity of the tryptophan 7-halogenase PrnA by site-directed mutagenesis. Angew Chem Int Edit 2011, 50:2951-2953.
54. Grüschow S., Rackham E.J., Elkins B., Newill P.L.A., Hill L.M., Goss R.J.M. New pacidamycin antibiotics through precursor-directed biosynthesis. Chembiochem 2009, 10:355-360.
55. Busche A., Gottstein D., Hein C., Ripin N., Pader I., Tufar P., Eisman E.B., Gu L.C., Walsh C.T., Sherman D.H., et al. Characterization of molecular interactions between ACP and halogenase domains in the curacin A polyketide synthase. ACS Chem Biol 2012, 7:377-385.
56. Zeng J., Zhan J.X. A novel fungal flavin-dependent halogenase for natural product biosynthesis. Chembiochem 2010, 11:2119-2123.
57. Wu Y.Y., Kang Q.J., Shen Y.M., Su W.J., Bai L.Q. Cloning and functional analysis of the naphthomycin biosynthetic gene cluster in Streptomyces sp CS. Mol Biosyst 2011, 7:2459-2469.
58. Foulston L.C., Bibb M.J. Microbisporicin gene cluster reveals unusual features of lantibiotic biosynthesis in actinomycetes. Proc Natl Acad Sci U S A 2010, 107:13461-13466.