Insights into the biosynthesis of 12-membered resorcylic acid lactones from heterologous production in saccharomyces cerevisiae

ACS Chemical Biology

Volumn 9, Issue 5, 2014, Pages 1119-1127

  Xu, Yuquan ^a,b   Zhou, Tong ^c   Espinosa Artiles, Patricia ^b   Tang, Ying ^b,d   Zhan, Jixun ^c   Molnár, István ^b,e  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b Environmental Research Laboratory   (United States)

^c Utah State University   (United States)

^d SICHUAN UNIVERSITY   (China)

^e UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; LACTONE; POLYKETIDE SYNTHASE; ALPHA-RESORCYLIC ACID; DESMETHYL-LASIODIPLODIN; HYDROXYBENZOIC ACID DERIVATIVE; LASIODIPLODIN; POLYKETIDE; RESORCINOL DERIVATIVE; ZEARALENONE;

ACREMONIUM; ACREMONIUM ZEAE; ARTICLE; BIOGENESIS; BIOSYNTHESIS; CONTROLLED STUDY; GENE LOCUS; GENE TRANSFER; GENETIC IDENTIFICATION; HETEROLOGOUS EXPRESSION; HOST; LASIODIPLODIA THEOBROMAE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; ANALOGS AND DERIVATIVES; CHEMISTRY; GENETIC ENGINEERING; GENETICS; METABOLISM; MOLECULAR GENETICS; PROCEDURES;

BIOSYNTHETIC PATHWAYS; GENETIC ENGINEERING; GENETIC LOCI; HYDROXYBENZOATES; LACTONES; MOLECULAR SEQUENCE DATA; POLYKETIDE SYNTHASES; POLYKETIDES; RESORCINOLS; SACCHAROMYCES CEREVISIAE; ZEARALENONE;

EID: 84900864845     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500043g     Document Type: Article

References (47)

1. Winssinger, N. and Barluenga, S. (2007) Chemistry and biology of resorcylic acid lactones Chem. Commun. 2007, 22-36
2. Xu, Y., Zhou, T., Zhou, Z., Su, S., Roberts, S. A., Montfort, W. R., Zeng, J., Chen, M., Zhang, W., Zhan, J., and Molnár, I. (2013) Rational reprogramming of fungal polyketide first-ring cyclization Proc. Natl. Acad. Sci. U.S.A. 110, 5398-5403
3. Thomas, R. (2001) A biosynthetic classification of fungal and streptomycete fused-ring aromatic polyketides ChemBioChem 2, 612-627
4. Winssinger, N., Fontaine, J. G., and Barluenga, S. (2009) Hsp90 inhibition with resorcyclic acid lactones (RALs) Curr. Top. Med. Chem. 9, 1419-1435
5. Schirmer, A., Kennedy, J., Murli, S., Reid, R., and Santi, D. V. (2006) Targeted covalent inactivation of protein kinases by resorcylic acid lactone polyketides Proc. Natl. Acad. Sci. U.S.A. 103, 4234-4239
6. Chooi, Y. H. and Tang, Y. (2012) Navigating the fungal polyketide chemical space: From genes to molecules J. Org. Chem. 77, 9933-9953
7. Li, Y., Xu, W., and Tang, Y. (2010) Classification, prediction, and verification of the regioselectivity of fungal polyketide synthase product template domains J. Biol. Chem. 285, 22764-22773
8. Crawford, J. M., Korman, T. P., Labonte, J. W., Vagstad, A. L., Hill, E. A., Kamari-Bidkorpeh, O., Tsai, S. C., and Townsend, C. A. (2009) Structural basis for biosynthetic programming of fungal aromatic polyketide cyclization Nature 461, 1139-1143
9. Wang, M., Zhou, H., Wirz, M., Tang, Y., and Boddy, C. N. (2009) A thioesterase from an iterative fungal polyketide synthase shows macrocyclization and cross coupling activity and may play a role in controlling iterative cycling through product offloading Biochemistry 48, 6288-6290
10. Xu, Y., Zhou, T., Zhang, S., Xuan, L. J., Zhan, J., and Molnár, I. (2013) Thioesterase domains of fungal nonreducing polyketide synthases act as decision gates during combinatorial biosynthesis J. Am. Chem. Soc. 135, 10783-10791
11. Gaffoor, I. and Trail, F. (2006) Characterization of two polyketide synthase genes involved in zearalenone biosynthesis in Gibberella zeae Appl. Environ. Microbiol. 72, 1793-1799
12. Wang, S., Xu, Y., Maine, E. A., Wijeratne, E. M. K., Espinosa-Artiles, P., Gunatilaka, A. A. L., and Molnár, I. (2008) Functional characterization of the biosynthesis of radicicol, an Hsp90 inhibitor resorcylic acid lactone from Chaetomium chiversii Chem. Biol. 15, 1328-1338
13. Reeves, C. D., Hu, Z., Reid, R., and Kealey, J. T. (2008) Genes for biosynthesis of the fungal polyketides hypothemycin from Hypomyces subiculosus and radicicol from Pochonia chlamydosporia Appl. Environ. Microbiol. 74, 5121-5129
14. Xu, Y., Espinosa-Artiles, P., Schubert, V., Xu, Y. M., Zhang, W., Lin, M., Gunatilaka, A. A. L., Sussmuth, R., and Molnár, I. (2013) Characterization of the biosynthetic genes for 10,11-dehydrocurvularin, a heat-shock response modulator anticancer fungal polyketide from Aspergillus terreus Appl. Environ. Microbiol. 79, 2038-2047
15. Zhou, H., Qiao, K., Gao, Z., Meehan, M. J., Li, J. W., Zhao, X., Dorrestein, P. C., Vederas, J. C., and Tang, Y. (2010) Enzymatic synthesis of resorcylic acid lactones by cooperation of fungal iterative polyketide synthases involved in hypothemycin biosynthesis J. Am. Chem. Soc. 132, 4530-4531
16. Zhou, H., Qiao, K., Gao, Z., Vederas, J. C., and Tang, Y. (2010) Insights into radicicol biosynthesis via heterologous synthesis of intermediates and analogs J. Biol. Chem. 285, 41412-41421
17. Yang, Q., Asai, M., Matsuura, H., and Yoshihara, T. (2000) Potato micro-tuber-inducing hydroxylasiodiplodins from Lasiodiplodia theobromae Phytochemistry 54, 489-494
18. Li, P., Takahashi, K., Matsuura, H., and Yoshihara, T. (2005) Novel potato micro-tuber-inducing compound, (3 R,6 S)-6-hydroxylasiodiplodin, from a strain of Lasiodiplodia theobromae Biosci. Biotechnol. Biochem. 69, 1610-1612
19. Veiga, T. A. M., Silva, S. C., Francisco, A.-C., Filho, E. R., Vieira, P. C., Fernandes, J. B., Silva, M. F. G. F., Mueller, M. W., and Lotina-Hennsen, B. (2007) Inhibition of photophosphorylation and electron transport chain in thylakoids by lasiodiplodin, a natural product from Botryosphaeria rhodina J. Agric. Food Chem. 55, 4217-4221
20. Buayairaksa, M., Kanokmedhakul, S., Kanokmedhakul, K., Moosophon, P., Hahnvajanawong, C., and Soytong, K. (2011) Cytotoxic lasiodiplodin derivatives from the fungus Syncephalastrum racemosum Arch. Pharmacal Res. 34, 2037-2041
21. Yao, X. S., Ebizuka, Y., Noguchi, H., Kiuchi, F., Shibuya, M., Iitaka, Y., Seto, H., and Sankawa, U. (1991) Biologically active constituents of Arnebia euchroma: structure of arnebinol, an ansa-type monoterpenylbenzenoid with inhibitory activity on prostaglandin biosynthesis Chem. Pharm. Bull. 39, 2956-2961
22. Jiang, C.-S., Zhou, R., Gong, J.-X., Chen, L.-L., Kurtan, T., Shen, X., and Guo, Y.-W. (2011) Synthesis, modification, and evaluation of (R)-de-O-methyllasiodiplodin and analogs as nonsteroidal antagonists of mineralocorticoid receptor Bioorg. Med. Chem. Lett. 21, 1171-1175
23. Lee, K. H., Hayashi, N., Okano, M., Hall, I. H., Wu, R. Y., and McPhail, A. T. (1982) Antitumor agents. Part 51. Lasiodiplodin, a potent antileukemic macrolide from Euphorbia splendens Phytochemistry 21, 1119-1121
24. Oyama, H., Sassa, T., and Ikeda, M. (1978) Structures of new plant growth inhibitors, trans-and cis-resorcylide Agric. Biol. Chem. 42, 2407-2409
25. Nukina, M., Sassa, T., Oyama, H., and Ikeda, M. (1979) Structures and biological activities of fungal macrolides, pyrenolide and resorcylide Koen Yoshishu-Tennen Yuki Kagobutsu Toronkai, 22nd 362-369
26. Poling, S. M., Wicklow, D. T., Rogers, K. D., and Gloer, J. B. (2008) Acremonium zeae, a protective endophyte of maize, produces dihydroresorcylide and 7-hydroxydihydroresorcylides J. Agric. Food Chem. 56, 3006-3009
27. Sassa, T., Nukina, M., and Ikeda, M. (1981) Electrophilic reactivities and biological activities of trans-and cis-resorcylides Nippon Kagaku Kaishi 1981, 883-885
28. West, R. R., Martinez, T., Franklin, H. R., Bishop, P. D., and Rassing, B. R. (1996) Cis-resorcylide, pharmaceutical composition containing it, and use thereof in the treatment of thrombosis and related disorders. (Zymogenetics, Inc., USA; Novo Nordisk A/S). Patent WO 9640671.
29. Kashima, T., Takahashi, K., Matsuura, H., and Nabeta, K. (2009) Biosynthesis of resorcylic acid lactone (5 S)-5-hydroxylasiodiplodin in Lasiodiplodia theobromae Biosci. Biotechnol. Biochem. 73, 2522-2524
30. Zhou, H., Gao, Z., Qiao, K., Wang, J., Vederas, J. C., and Tang, Y. (2012) A fungal ketoreductase domain that displays substrate-dependent stereospecificity Nat. Chem. Biol. 8, 331-333
31. Ma, S. M., Li, J. W., Choi, J. W., Zhou, H., Lee, K. K., Moorthie, V. A., Xie, X., Kealey, J. T., Da Silva, N. A., Vederas, J. C., and Tang, Y. (2009) Complete reconstitution of a highly reducing iterative polyketide synthase Science 326, 589-592
32. Zhou, H., Zhan, J., Watanabe, K., Xie, X., and Tang, Y. (2008) A polyketide macrolactone synthase from the filamentous fungus Gibberella zeae Proc. Natl. Acad. Sci. U.S.A. 105, 6249-6254
33. Zhang, L., Ma, W., Xu, L., Deng, F., and Guo, Y. (2013) Efficient total synthesis of (S)-dihydroresorcylide, a bioactive twelve-membered macrolide Chin. J. Chem. 31, 339-343
34. Matsuura, H., Nakamori, K., Omer, E. A., Hatakeyama, C., Yoshihara, T., and Ichihara, A. (1998) Three lasiodiplodins from Lasiodiplodia theobromae IFO 31059 Phytochemistry 49, 579-584
35. Zheng, J., Taylor, C. A., Piasecki, S. K., and Keatinge-Clay, A. T. (2010) Structural and functional analysis of A-type ketoreductases from the amphotericin modular polyketide synthase Structure 18, 913-922
36. Gao, J., Radwan, M. M., Leon, F., Dale, O. R., Husni, A. S., Wu, Y., Lupien, S., Wang, X., Manly, S. P., Hill, R. A., Dugan, F. M., Cutler, H. G., and Cutler, S. J. (2013) Neocosmospora sp.-derived resorcylic acid lactones with in vitro binding affinity for human opioid and cannabinoid receptors J. Nat. Prod. 76, 824-828
37. Crawford, J. M., Vagstad, A. L., Ehrlich, K. C., and Townsend, C. A. (2008) Starter unit specificity directs genome mining of polyketide synthase pathways in fungi Bioorg. Chem. 36, 16-22
38. Bali, S., OHare, H. M., and Weissman, K. J. (2006) Broad substrate specificity of ketoreductases derived from modular polyketide synthases ChemBioChem 7, 478-484
39. Ahuja, M., Chiang, Y. M., Chang, S. L., Praseuth, M. B., Entwistle, R., Sanchez, J. F., Lo, H. C., Yeh, H. H., Oakley, B. R., and Wang, C. C. (2012) Illuminating the diversity of aromatic polyketide synthases in Aspergillus nidulans J. Am. Chem. Soc. 134, 8212-8221
40. Ayer, W. A. and Pena-Rodriguez, L. (1987) Minor metabolites of Monocillium nordinii Phytochemistry 26, 1353-1355
41. Galimberti, E., Cerutti, S., and Forlani, A. (1975) Action of an antiandrogen on ontogenesis in the rat Boll. Chim. Farm. 114, 169-182
42. Moss, S. J., Martin, C. J., and Wilkinson, B. (2004) Loss of co-linearity by modular polyketide synthases: A mechanism for the evolution of chemical diversity Nat. Prod. Rep. 21, 575-593
43. He, J. and Hertweck, C. (2003) Iteration as programmed event during polyketide assembly; molecular analysis of the aureothin biosynthesis gene cluster Chem. Biol. 10, 1225-1232
44. Bruheim, P., Borgos, S. E. F., Tsan, P., Sletta, H., Ellingsen, T. E., Lancelin, J.-M., and Zotchev, S. B. (2004) Chemical diversity of polyene macrolides produced by Streptomyces noursei ATCC 11455 and recombinant strain ERD44 with genetically altered polyketide synthase NysC Antimicrob. Agents Chemother. 48, 4120-4129
45. Vagstad, A. L., Hill, E. A., Labonte, J. W., and Townsend, C. A. (2012) Characterization of a fungal thioesterase having Claisen cyclase and deacetylase activities in melanin biosynthesis Chem. Biol. 19, 1525-1534
46. Christianson, T. W., Sikorski, R. S., Dante, M., Shero, J. H., and Hieter, P. (1992) Multifunctional yeast high-copy-number shuttle vectors Gene 110, 119-122
47. Udwary, D. W., Merski, M., and Townsend, C. A. (2002) A method for prediction of the locations of linker regions within large multifunctional proteins, and application to a type I polyketide synthase J. Mol. Biol. 323, 585-598