Structure and Mechanism of the Magnesium-Independent Aromatic Prenyltransferase CloQ from the Clorobiocin Biosynthetic Pathway

Journal of Molecular Biology

Volumn 404, Issue 4, 2010, Pages 611-626

  Metzger, Ute ^a,b   Keller, Sascha ^a   Stevenson, Clare E M ^a   Heide, Lutz ^b   Lawson, David M ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Antibiotic; Crystal structure; PT fold; Site directed mutagenesis; Streptomyces

Indexed keywords

ANTIBIOTIC AGENT; CLOROBIOCIN; DIMETHYLALLYLTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CATALYSIS; CRYSTAL STRUCTURE; DRUG MECHANISM; DRUG SPECIFICITY; DRUG STRUCTURE; ENZYME ACTIVITY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STREPTOMYCES; STREPTOMYCES ROSEOCHROMOGENES;

STREPTOMYCES; STREPTOMYCES ROSEOCHROMOGENES SUBSP. OSCITANS;

EID: 78549293840     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.09.067     Document Type: Article

References (48)

1. Heide L. Prenyl transfer to aromatic substrates: genetics and enzymology. Curr. Opin. Chem. Biol. 2009, 13:171-179.
2. Poulter C.D. Farnesyl diphosphate synthase. A paradigm for understanding structure and function relationships in E-polyprenyl diphosphate synthases. Phytochem. Rev. 2006, 5:17-26.
3. Brauer L., Brandt W., Schulze D., Zakharova S., Wessjohann L. A structural model of the membrane-bound aromatic prenyltransferase UbiA from E. coli. ChemBioChem 2008, 9:982-992.
4. Steffan N., Grundmann A., Yin W.B., Kremer A., Li S.M. Indole prenyltransferases from fungi: a new enzyme group with high potential for the production of prenylated indole derivatives. Curr. Med. Chem. 2009, 16:218-231.
5. Edwards D.J., Gerwick W.H. Lyngbyatoxin biosynthesis: sequence of biosynthetic gene cluster and identification of a novel aromatic prenyltransferase. J. Am. Chem. Soc. 2004, 126:11432-11433.
6. Schultz A.W., Lewis C.A., Luzung M.R., Baran P.S., Moore B.S. Functional characterization of the cyclomarin/cyclomarazine prenyltransferase CymD directs the biosynthesis of unnatural cyclic peptides. J. Nat. Prod. 2010, 73:373-377.
7. Saleh O., Haagen Y., Seeger K., Heide L. Prenyl transfer to aromatic substrates in the biosynthesis of aminocoumarins, meroterpenoids and phenazines: the ABBA prenyltransferase family. Phytochemistry 2009, 70:1728-1738.
8. Tello M., Kuzuyama T., Heide L., Noel J.P., Richard S.B. The ABBA family of aromatic prenyltransferases: broadening natural product diversity. Cell Mol. Life Sci. 2008, 65:1459-1463.
9. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
10. Soding J., Biegert A., Lupas A.N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005, 33:W244-W248.
11. Kuzuyama T., Noel J.P., Richard S.B. Structural basis for the promiscuous biosynthetic prenylation of aromatic natural products. Nature 2005, 435:983-987.
12. Metzger U., Schall C., Zocher G., Unsold I., Stec E., Li S.M., et al. The structure of dimethylallyl tryptophan synthase reveals a common architecture of aromatic prenyltransferases in fungi and bacteria. Proc. Natl Acad. Sci. USA 2009, 106:14309-14314.
13. 8-barrel enzymes. Curr. Opin. Chem. Biol. 2003, 7:252-264.
14. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
15. Haug-Schifferdecker E., Arican D., Bruckner R., Heide L. A new group of aromatic prenyltransferases in fungi, catalyzing a 2,7-dihydroxynaphthalene 3-dimethylallyl-transferase reaction. J. Biol. Chem. 2010, 285:16487-16494.
16. Haagen Y., Glück K., Fay K., Kammerer B., Gust B., Heide L. A gene cluster for prenylated naphthoquinone and prenylated phenazine biosynthesis in Streptomyces cinnamonensis DSM 1042. ChemBioChem 2006, 7:2016-2027.
17. Kumano T., Richard S.B., Noel J.P., Nishiyama M., Kuzuyama T. Chemoenzymatic syntheses of prenylated aromatic small molecules using Streptomyces prenyltransferases with relaxed substrate specificities. Bioorg. Med. Chem. 2008, 16:8117-8126.
18. Saleh O., Gust B., Boll B., Fiedler H.P., Heide L. Aromatic prenylation in phenazine biosynthesis: dihydrophenazine-1-carboxylate dimethylallyltransferase from Streptomyces anulatus. J. Biol. Chem. 2009, 284:14439-14447.
19. Pojer F., Wemakor E., Kammerer B., Chen H., Walsh C.T., Li S.M., Heide L. CloQ, a prenyltransferase involved in clorobiocin biosynthesis. Proc. Natl Acad. Sci. USA 2003, 100:2316-2321.
20. Ozaki T., Mishima S., Nishiyama M., Kuzuyama T. NovQ is a prenyltransferase capable of catalyzing the addition of a dimethylallyl group to both phenylpropanoids and flavonoids. J. Antibiot. (Tokyo) 2009, 62:385-392.
21. Maxwell A., Lawson D.M. The ATP-binding site of type II topoisomerases as a target for antibacterial drugs. Curr. Top. Med. Chem. 2003, 3:283-303.
22. Heide L. The aminocoumarins: biosynthesis and biology. Nat. Prod. Rep. 2009, 26:1241-1250.
23. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The Protein Data Bank. Nucleic Acids Res. 2000, 28:235-242.
24. Holm L., Sander C. DALI: a network tool for protein structure comparison. Trends Biochem. Sci. 1995, 20:478-480.
25. Krissinel E., Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. Sect. D 2004, 60:2256-2268.
26. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
27. Keller S., Pojer F., Heide L., Lawson D.M. Crystallization and preliminary X-ray analysis of the aromatic prenyltransferase CloQ from the clorobiocin biosynthetic cluster of Streptomyces roseochromogenes. Acta Crystallogr. Sect. F 2006, 62:1153-1155.
28. Unsöld I.A., Li S.M. Overproduction, purification and characterization of FgaPT2, a dimethylallyltryptophan synthase from Aspergillus fumigatus. Microbiology 2005, 151:1499-1505.
29. Gebler J.C., Woodside A.B., Poulter C.D. Dimethylallyltryptophan synthase. An enzyme-catalyzed electrophilic aromatic substitution. J. Am. Chem. Soc. 1992, 114:7354-7360.
30. Degenhardt J., Kollner T.G., Gershenzon J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 2009, 70:1621-1637.
31. Chi Y., Duan J., Qi X., Chen G. Electrochemical study on the keto-enol tautomerization of p-hydroxyphenylpyruvic acid in aqueous solution. Bioelectrochemistry 2003, 60:37-45.
32. Doy C.H. Alkaline conversion of 4-hydroxyphenylpyruvic acid to 4-hydroxybenzaldehyde. Nature 1960, 186:529-531.
33. Schwarz K. Separation of enol and keto tautomers of aromatic pyruvic acids by paper chromatography. Arch. Biochem. Biophys. 1961, 92:168-175.
34. Sambrook J., Russell D.W. Molecular Cloning. A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York. NY.
35. Leslie A.G. The integration of macromolecular diffraction data. Acta Crystallogr. Sect. D 2006, 62:48-57.
36. Evans P. Scaling and assessment of data quality. Acta Crystallogr. Sect. D 2006, 62:72-82.
37. Dauter Z., Dauter M., Rajashankar K.R. Novel approach to phasing proteins: derivatization by short cryo-soaking with halides. Acta Crystallogr. Sect. D. 2000, 56:232-237.
38. Evans G., Bricogne G. Triiodide derivatization and combinatorial counter-ion replacement: two methods for enhancing phasing signal using laboratory Cu Kα X-ray equipment. Acta Crystallogr. Sect. D 2002, 58:976-991.
39. Sheldrick G.M. A short history of SHELX. Acta Crystallogr. Sect. A 2008, 64:112-122.
40. Pape T., Schneider T.R. HKL2MAP: a graphical user interface for phasing with SHELX programs. J. Appl. Crystallogr. 2004, 37:843-844.
41. Cowtan K. DM: an automated procedure for phase improvement by density modification. Jt. CCP4 ESF-EACBM Newsl. Protein Crystallogr 1994, 31:34-38.
42. Perrakis A., Morris R., Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 1999, 6:458-463.
43. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D. 2004, 60:2126-2132.
44. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D 1997, 53:240-255.
45. Read R.J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr. Sect. A 1986, 42:140-149.
46. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
47. DeLano W.L. The PyMOL User's Manual 2002, DeLano Scientific, San Carlos, CA.
48. Woodside A.B., Huang Z., Poulter C.D. Trisammonium geranyl diphosphate [diphosphoric acid, mono(3,7-dimethyl-2,6-octadienyl) ester (E)-, trisammonium salt]. Org. Synth. 1988, 66:211.