Biochemical characterization of indole prenyltransferases: Filling the lastgapofprenylation positions bya5-dimethylallyltryptophan synthase from aspergillus clavatus

Journal of Biological Chemistry

Volumn 287, Issue 2, 2012, Pages 1371-1380

  Yu, Xia ^a   Liu, Yan ^a,b   Xie, Xiulan ^a   Zheng, Xiao Dong ^b   Li, Shu Ming ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC SUBSTRATES; BIOCHEMICAL CHARACTERIZATION; CATALYTIC EFFICIENCIES; CHEMO-ENZYMATIC SYNTHESIS; CONVERSION YIELD; DI-PEPTIDES; DIPHOSPHATES; ENZYME PRODUCTS; FARNESYL DIPHOSPHATE; GENOME SEQUENCES; HIS-TAGGED PROTEINS; INDOLE DERIVATIVES; KINETIC DATA; L-TRYPTOPHAN; PRENYLATION; PRENYLTRANSFERASE; PRODUCT FORMATION; REACTION MIXTURE; RECOMBINANT ENZYMES; REGIOSPECIFIC; STRUCTURE ELUCIDATION; SYNTHASES; TURNOVER NUMBER;

ASPERGILLUS; ENZYME ACTIVITY; ESCHERICHIA COLI; GENES; SUBSTRATES; SYNTHESIS (CHEMICAL);

AMINO ACIDS;

5 DIMETHYLALLYLTRYPOPHAN SYNTHASE; DIMETHYLALLYL DIPHOSPHATE; DIMETHYLALLYLTRANSFERASE; FARNESYL DIPHOSPHATE; GERANYL DIPHOSPHATE; HISTONE; INDOLE DERIVATIVE; INDOLE DIMETHYLALLYLTRANSFERASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ACLA 031240 GENE; ARTICLE; ASPERGILLUS; ASPERGILLUS CLAVATUS; BIOCHEMISTRY; CATALYSIS; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENZYME KINETICS; ENZYME SYNTHESIS; ESCHERICHIA COLI; FUNGAL GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PRENYLATION; PROTEIN PURIFICATION;

ASPERGILLUS; CATALYSIS; DIMETHYLALLYLTRANSTRANSFERASE; ESCHERICHIA COLI; FUNGAL PROTEINS; HEMITERPENES; ORGANOPHOSPHORUS COMPOUNDS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

ASPERGILLUS CLAVATUS; ESCHERICHIA COLI;

EID: 84862907862     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.317982     Document Type: Article

References (52)

1. Li, S. M. (2010) Prenylated indole derivatives from fungi. Structure diversity, biological activities, biosynthesis, and chemoenzymatic synthesis. Nat. Prod. Rep. 27, 57-78
2. Ruiz-Sanchis, P., Savina, S. A., Albericio, F., and Álvarez, M. (2011) Structure, bioactivity, and synthesis of natural products with hexahydropyrrolo[ 2,3-b]indole. Chemistry 17, 1388-1408
3. Wallwey, C., and Li, S. M. (2011) Ergot alkaloids. Structure diversity, biosynthetic gene clusters, and functional proof of biosynthetic genes. Nat. Prod. Rep. 28, 496-510
4. Lindel, T., Marsch, N., and Adla, S. K. (2011) Indole prenylation in alkaloid synthesis. Top. Curr. Chem. DOI: 10.1007/128-2011-204
5. Williams, R. M., Stocking, E. M., and Sanz-Cervera, J. F. (2000) Biosynthesis of prenylated alkaloids derived from tryptophan. Top. Curr. Chem. 209, 97-173
6. Schardl, C. L., Panaccione, D. G., and Tudzynski, P. (2006) Ergot alkaloids, biology and molecular biology. Alkaloids Chem. Biol. 63, 45-86
7. Uhlig, S., Botha, C. J., Vrålstad, T., Rolén, E., and Miles, C. O. (2009) Indole-diterpenes and ergot alkaloids in Cynodon dactylon (Bermuda grass) infected with Claviceps cynodontis from an outbreak of tremors in cattle. J. Agric. Food Chem. 57, 11112-11119
8. Heide, L. (2009) Prenyl transfer to aromatic substrates. Genetics and enzymology. Curr. Opin. Chem. Biol. 13, 171-179
9. Yazaki, K., Sasaki, K., and Tsurumaru, Y. (2009) Prenylation of aromatic compounds, a key diversification of plant secondary metabolites. Phytochemistry 70, 1739-1745
10. Yin, W. B., Yu, X., Xie, X. L., and Li, S. M. (2010) Preparation of pyrrolo[ 2,3-b]indoles carrying a β-configured reverse C3-dimethylallyl moiety by using a recombinant prenyltransferase CdpC3PT. Org. Biomol. Chem. 8, 2430-2438
11. Zou, H. X., Xie, X. L., Linne, U., Zheng, X. D., and Li, S. M. (2010) Simultaneous C7- and N1-prenylation of cyclo-L-Trp-L-Trp catalyzed by a prenyltransferase from Aspergillus oryzae. Org. Biomol. Chem. 8, 3037-3044
12. Schultz, A. W., Lewis, C. A., Luzung, M. R., Baran, P. S., and Moore, B. S. (2010) Functional characterization of the cyclomarin/cyclomarazine prenyltransferase CymD directs the biosynthesis of unnatural cyclic peptides. J. Nat. Prod. 73, 373-377
13. Takahashi, S., Takagi, H., Toyoda, A., Uramoto, M., Nogawa, T., Ueki, M., Sakaki, Y., and Osada, H. (2010) Biochemical characterization of a novel indole prenyltransferase from Streptomyces sp. SN-593. J. Bacteriol. 192, 2839-2851
14. Ding, Y., de Wet, J. R., Cavalcoli, J., Li, S., Greshock, T. J., Miller, K. A., Finefield, J. M., Sunderhaus, J. D., McAfoos, T. J., Tsukamoto, S., Williams, R. M., and Sherman, D. H. (2010) Genome-based characterization of two prenylation steps in the assembly of the stephacidin and notoamide anticancer agents in a marine-derived Aspergillus sp. J. Am. Chem. Soc. 132, 12733-12740
15. Li, S. M. (2009) Evolution of aromatic prenyltransferases in the biosynthesis of indole derivatives. Phytochemistry 70, 1746-1757
16. Grundmann, A., Kuznetsova, T., Afiyatullov, S. Sh., and Li, S. M. (2008) FtmPT2, anN-prenyltransferase from Aspergillus fumigatus, catalyzes the last step in the biosynthesis of fumitremorgin B. ChemBioChem 9, 2059-2063
17. Grundmann, A., and Li, S. M. (2005) Overproduction, purification, and characterization of FtmPT1, a brevianamide F prenyltransferase from Aspergillus fumigatus. Microbiology 151, 2199-2207 (Pubitemid 40984293)
18. Unsöld, I. A., and Li, S. M. (2006) Reverse prenyltransferase in the biosynthesis of fumigaclavine C in Aspergillus fumigatus. Gene expression, purification, and characterization of fumigaclavine C synthase FGAPT1. ChemBioChem 7, 158-164 (Pubitemid 43076299)
19. Yin, W. B., Grundmann, A., Cheng, J., and Li, S. M. (2009) Acetylaszonalenin biosynthesis in Neosartorya fischeri. Identification of the biosynthetic gene cluster by genomic mining and functional proof of the genes by biochemical investigation. J. Biol. Chem. 284, 100-109
20. Unsöld, I. A., and Li, S. M. (2005) Overproduction, purification, and characterization of FgaPT2, a dimethylallyltryptophan synthase from Aspergillus fumigatus. Microbiology 151, 1499-1505 (Pubitemid 40711797)
21. Liu, X., and Walsh, C. T. (2009) Characterization of cyclo-acetoacetyl- Ltryptophan dimethylallyltransferase in cyclopiazonic acid biosynthesis. Substrate promiscuity and site -directed mutagenesis studies. Biochemistry 48, 11032-11044
22. Kremer, A., Westrich, L., and Li, S. M. (2007)A7-dimethylallyltryptophan synthase from Aspergillus fumigatus. Overproduction, purification, and biochemical characterization. Microbiology 153, 3409-3416 (Pubitemid 47629546)
23. Achenbach, H., Renner, C., and Waibel, R. (1995) Constituents of tropical medicinal plants, LXIX. The hexalobines, diprenylated indoles from Hexalobus crispiflorus and Hexalobus monopetalus. Liebigs Ann. Recl. 1995, 1327-1337
24. Peters, L., König, G. M., Terlau, H., and Wright, A. D. (2002) Four new bromotryptamine derivatives from the marine bryozoan Flustra foliacea. J. Nat. Prod. 65, 1633-1637 (Pubitemid 35386793)
25. Fredenhagen, A., Petersen, F., Tintelnot-Blomley, M., Rösel, J., Mett, H., and Hug, P. (1997) Semicochliodinol A and B. Inhibitors of HIV-1 protease and EGF-R protein-tyrosine kinase related to asterriquinones produced by the fungus Chrysosporium merdarium. J. Antibiot. 50, 395-401 (Pubitemid 27254681)
26. Ooike, M., Nozawa, K., Udagawa, S I., and Kawai, K. I. (1997) Bisindolylbenzenoids from ascostromata of Petromyces muricatus. Can. J. Chem. 75, 625-628 (Pubitemid 127498030)
27. Balibar, C. J., Howard-Jones, A. R., and Walsh, C. T. (2007) Terrequinone A biosynthesis through L-tryptophan oxidation, dimerization and bisprenylation. Nat. Chem. Biol. 3, 584-592 (Pubitemid 47294397)
28. Wang, W. L., Lu, Z. Y., Tao, H. W., Zhu, T. J., Fang, Y. C., Gu, Q. Q., and Zhu, W. M. (2007) Isoechinulin-type alkaloids, variecolorins A-L, from halotolerant Aspergillus variecolor. J. Nat. Prod. 70, 1558-1564
29. Fujimoto, H., Fujimaki, T., Okuyama, E., and Yamazaki, M. (1999) Immunomodulatory constituents from an ascomycete, Microascus tardifaciens. Chem. Pharm. Bull. 47, 1426-1432 (Pubitemid 29510311)
30. Xu, M., Gessner, G., Groth, I., Lange, C., Christner, A., Bruhn, T., Deng, Z., Li, X., Heinemann, S. H., Grabley, S., Bringmann, G., Sattler, I., and Lin, W. (2007) Shearinines D-K, new indole triterpenoids from an endophytic Penicillium sp. (strain HKI0459) with blocking activity on large-conductance calcium-activated potassium channels. Tetrahedron 63, 435-444 (Pubitemid 44838787)
31. Sings, H., and Singh, S. (2003) Tremorgenic and nontremorgenic 2,3- fused indole diterpenoids. Alkaloids Chem. Biol. 60, 51-163 (Pubitemid 137640335)
32. Belofsky, G. N., Gloer, J. B., Wicklow, D. T., and Dowd, P. F. (1995) Antiinsectan alkaloids: Shearinines A-C and a new paxilline derivative from the ascostromata of Eupenicillium shearii. Tetrahedron 51, 3959-3968
33. Woodside, A. B., Huang, Z., and Poulter, C. D. (1988) Trisammonium geranyl diphosphate. Org. Synth. 66, 211-215
34. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
35. Berger, S., and Braun, S. (2004) 200 and More NMR Experiments. A Practical Course, pp. 1-854, Wiley-VCH, Weinheim, Germany
36. Steffan, N., and Li, S. M. (2009) Increasing structure diversity of prenylated diketopiperazine derivatives by using a 4-dimethylallyltryptophan synthase. Arch. Microbiol. 191, 461-466
37. Steffan, N., Unsöld, I. A., and Li, S. M. (2007) Chemoenzymatic synthesis of prenylated indole derivatives by using a 4-dimethylallyltryptophan synthase from Aspergillus fumigatus. ChemBioChem 8, 1298-1307 (Pubitemid 47171997)
38. Kremer, A., and Li, S. M. (2008) Potential of a 7-dimethylallyltryptophan synthase as a tool for production of prenylated indole derivatives. Appl. Microbiol. Biotechnol. 79, 951-961
39. Steffan, N., Grundmann, A., Yin, W. B., Kremer, A., and Li, S. M. (2009) Indole prenyltransferases from fungi. A new enzyme group with high potential for the production of prenylated indole derivatives. Curr. Med. Chem. 16, 218-231
40. Li, S. M. (2009) Applications of dimethylallyltryptophan synthases and other indole prenyltransferases for structural modification of natural products. Appl. Microbiol. Biotechnol. 84, 631-639
41. Liang, P. H. (2009) Reaction kinetics, catalytic mechanisms, conformational changes, and inhibitor design for prenyltransferases. Biochemistry 48, 6562-6570
42. Turunen, M., Olsson, J., and Dallner, G. (2004) Metabolism and function of coenzyme Q. Biochim. Biophys. Acta 1660, 171-199 (Pubitemid 38125244)
43. Sacchettini, J. C., and Poulter, C. D. (1997) Creating isoprenoid diversity. Science 277, 1788-1789 (Pubitemid 27449183)
44. Nielsen, K. F., and Smedsgaard, J. (2003) Fungal metabolite screening. Database of 474 mycotoxins and fungal metabolites for dereplication by standardized liquid chromatography-UV-mass spectrometry methodology. J. Chromatogr. A 1002, 111-136 (Pubitemid 36700450)
45. Edwards, D. J., and Gerwick, W. H. (2004) Lyngbyatoxin biosynthesis. Sequence of biosynthetic gene cluster and identification of a novel aromatic prenyltransferase. J. Am. Chem. Soc. 126, 11432-11433 (Pubitemid 39244947)
46. Yu, X., Xie, X., and Li, S. M. (2011) Substrate promiscuity of secondary metabolite enzymes: prenylation of hydroxynaphthalenes by fungal indole prenyltransferases. Appl. Microbiol. Biotechnol. 92, 737-748
47. Yu, X., and Li, S. M. (2011) Prenylation of flavonoids by using a dimethylallyltryptophan synthase 7-DMATS from Aspergillus fumigatus. Chem- BioChem 12, 2280-2283
48. Machida, M., Asai, K., Sano, M., Tanaka, T., Kumagai, T., Terai, G., Kusumoto, K., Arima, T., Akita, O., Kashiwagi, Y., Abe, K., Gomi, K., Horiuchi, H., Kitamoto, K., Kobayashi, T., Takeuchi, M., Denning, D. W., Galagan, J. E., Nierman, W. C., Yu, J., Archer, D. B., Bennett, J. W., Bhatnagar, D., Cleveland, T. E., Fedorova, N. D., Gotoh, O., Horikawa, H., Hosoyama, A., Ichinomiya, M., Igarashi, R., Iwashita, K., Juvvadi, P. R., Kato, M., Kato, Y., Kin, T., Kokubun, A., Maeda, H., Maeyama, N., Maruyama, J., Nagasaki, H., Nakajima, T., Oda, K., Okada, K., Paulsen, I., Sakamoto, K., Sawano, T., Takahashi, M., Takase, K., Terabayashi, Y., Wortman, J. R., Yamada, O., Yamagata, Y., Anazawa, H., Hata, Y., Koide, Y., Komori, T., Koyama, Y., Minetoki, T., Suharnan, S., Tanaka, A., Isono, K., Kuhara, S., Ogasawara, N., and Kikuchi, H. (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438, 1157-1161 (Pubitemid 41831685)
49. Cleveland, T. E., Yu, J., Fedorova, N., Bhatnagar, D., Payne, G. A., Nierman, W. C., and Bennett, J. W. (2009) Potential of Aspergillus flavus genomics for applications in biotechnology. Trends Biotechnol. 27, 151-157
50. Ding, Y., Williams, R. M., and Sherman, D. H. (2008) Molecular analysis of a 4-dimethylallyltryptophan synthase from Malbranchea aurantiaca. J. Biol. Chem. 283, 16068-16076
51. Markert, A., Steffan, N., Ploss, K., Hellwig, S., Steiner, U., Drewke, C., Li, S. M., Boland, W., and Leistner, E. (2008) Biosynthesis and accumulation of ergoline alkaloids in a mutualistic association between Ipomoea asarifolia (Convolvulaceae) and a clavicipitalean fungus. Plant Physiol. 147, 296-305 (Pubitemid 352844368)
52. Steiner, U., Leibner, S., Schardl, C. L., Leuchtmann, A., and Leistner, E. (2011) Periglandula, a new fungal genus within the Clavicipitaceae and its association with Convolvulaceae. Mycologia 103, 1133-1145