Structural and functional analysis of the loading acyltransferase from avermectin modular polyketide synthase

ACS Chemical Biology

Volumn 10, Issue 4, 2015, Pages 1017-1025

  Wang, Fen ^a   Wang, Yanjie ^a   Ji, Junjie ^a   Zhou, Zhan ^a   Yu, Jingkai ^a   Zhu, Hua ^b   Su, Zhiguo ^a   Zhang, Lixin ^b   Zheng, Jianting ^a  

^a INSTITUTE OF PROCESS ENGINEERING   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYLBUTYRIC ACID; AVERMECTIN; CARBOXYLIC ACID DERIVATIVE; POLYKETIDE SYNTHASE; THIOXYL DERIVATIVE; 2-METHYLBUTANOIC ACID; ACYLTRANSFERASE; BUTYRIC ACID DERIVATIVE; IVERMECTIN;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ENGINEERING; ENZYME SUBSTRATE; HYDROLYSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SITE DIRECTED MUTAGENESIS; STEREOSPECIFICITY; ANALOGS AND DERIVATIVES; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROCEDURES; PROTEIN ENGINEERING; PROTEIN TERTIARY STRUCTURE; STEREOISOMERISM; STREPTOMYCES; X RAY CRYSTALLOGRAPHY;

ACYLTRANSFERASES; BASE SEQUENCE; BUTYRATES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HYDROLYSIS; IVERMECTIN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYKETIDE SYNTHASES; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; STEREOISOMERISM; STREPTOMYCES; SUBSTRATE SPECIFICITY;

EID: 84928116281     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500873k     Document Type: Article

References (41)

1. Khosla, C., Herschlag, D., Cane, D. E., and Walsh, C. T. (2014) Assembly line polyketide synthases: Mechanistic insights and unsolved problems Biochemistry 53, 2875-2883
2. Xu, W., Qiao, K., and Tang, Y. (2013) Structural analysis of protein-protein interactions in type I polyketide synthases Crit. Rev. Biochem. Mol. Biol. 48, 98-122
3. Dutta, S., Whicher, J. R., Hansen, D. A., Hale, W. A., Chemler, J. A., Congdon, G. R., Narayan, A. R., Hakansson, K., Sherman, D. H., Smith, J. L., and Skiniotis, G. (2014) Structure of a modular polyketide synthase Nature 510, 512-517
4. Zhuo, Y., Zhang, T., Wang, Q., Cruz-Morales, P., Zhang, B., Liu, M., Barona-Gomez, F., and Zhang, L. (2014) Synthetic biology of avermectin for production improvement and structure diversification Biotechnol. J. 9, 316-325
5. Dutton, C. J., Gibson, S. P., Goudie, A. C., Holdom, K. S., Pacey, M. S., Ruddock, J. C., BuLock, J. D., and Richards, M. K. (1991) Novel avermectins produced by mutational biosynthesis J. Antibiot. (Tokyo) 44, 357-365
6. Marsden, A. F. A., Wilkinson, B., Cortes, J., Dunster, N. J., Staunton, J., and Leadlay, P. F. (1998) Engineering broader specificity into an antibiotic-producing polyketide synthase Science 279, 199-202
7. Lau, J., Cane, D. E., and Khosla, C. (2000) Substrate specificity of the loading didomain of the erythromycin polyketide synthase Biochemistry 39, 10514-10520
8. Yuzawa, S., Eng, C. H., Katz, L., and Keasling, J. D. (2013) Broad substrate specificity of the loading didomain of the lipomycin polyketide synthase Biochemistry 52, 3791-3793
9. Bisang, C., Long, P. F., Cortes, J., Westcott, J., Crosby, J., Matharu, A. L., Cox, R. J., Simpson, T. J., Staunton, J., and Leadlay, P. F. (1999) A chain initiation factor common to both modular and aromatic polyketide synthases Nature 401, 502-505
10. Long, P. F., Wilkinson, C. J., Bisang, C. P., Cortes, J., Dunster, N., Oliynyk, M., McCormick, E., McArthur, H., Mendez, C., Salas, J. A., Staunton, J., and Leadlay, P. F. (2002) Engineering specificity of starter unit selection by the erythromycin-producing polyketide synthase Mol. Microbiol. 43, 1215-1225
11. Oefner, C., Schulz, H., DArcy, A., and Dale, G. E. (2006) Mapping the active site of Escherichia coli malonyl-CoA-acyl carrier protein transacylase (FabD) by protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 613-618
12. Tang, Y., Chen, A. Y., Kim, C. Y., Cane, D. E., and Khosla, C. (2007) Structural and mechanistic analysis of protein interactions in module 3 of the 6-deoxyerythronolide B synthase Chem. Biol. 14, 931-943
13. Tang, Y., Kim, C. Y., Mathews, II, Cane, D. E., and Khosla, C. (2006) The 2.7-Å crystal structure of a 194-kDa homodimeric fragment of the 6-deoxyerythronolide B synthase Proc. Natl. Acad. Sci. U.S.A. 103, 11124-11129
14. Chen, A. Y., Cane, D. E., and Khosla, C. (2007) Structure-based dissociation of a type I polyketide synthase module Chem. Biol. 14, 784-792
15. Castonguay, R., He, W., Chen, A. Y., Khosla, C., and Cane, D. E. (2007) Stereospecificity of ketoreductase domains of the 6-deoxyerythronolide B synthase J. Am. Chem. Soc. 129, 13758-13769
16. Hagen, A., Poust, S., de Rond, T., Yuzawa, S., Katz, L., Adams, P. D., Petzold, C. J., and Keasling, J. D. (2014) In vitro analysis of carboxyacyl substrate tolerance in the loading and first extension modules of Borrelidin PKS Biochemistry 53, 5975-5977
17. Bergeret, F., Gavalda, S., Chalut, C., Malaga, W., Quemard, A., Pedelacq, J. D., Daffe, M., Guilhot, C., Mourey, L., and Bon, C. (2012) Biochemical and structural study of the atypical acyltransferase domain from the mycobacterial polyketide synthase Pks13 J. Biol. Chem. 287, 33675-33690
18. Keatinge-Clay, A. T., Shelat, A. A., Savage, D. F., Tsai, S. C., Miercke, L. J., OConnell, J. D., Khosla, C., and Stroud, R. M. (2003) Catalysis, specificity, and ACP docking site of Streptomyces coelicolor malonyl-CoA:ACP transacylase Structure 11, 147-154
19. Liew, C. W., Nilsson, M., Chen, M. W., Sun, H., Cornvik, T., Liang, Z. X., and Lescar, J. (2012) Crystal structure of the acyltransferase domain of the iterative polyketide synthase in enediyne biosynthesis J. Biol. Chem. 287, 23203-23215
20. Maier, T., Leibundgut, M., and Ban, N. (2008) The crystal structure of a mammalian fatty acid synthase Science 321, 1315-1322
21. Wong, F. T., Jin, X., Mathews, II, Cane, D. E., and Khosla, C. (2011) Structure and mechanism of the trans-acting acyltransferase from the disorazole synthase Biochemistry 50, 6539-6548
22. Whicher, J. R., Smaga, S. S., Hansen, D. A., Brown, W. C., Gerwick, W. H., Sherman, D. H., and Smith, J. L. (2013) Cyanobacterial polyketide synthase docking domains: A tool for engineering natural product biosynthesis Chem. Biol. 20, 1340-1351
23. Liang, J., Edelsbrunner, H., and Woodward, C. (1998) Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design Protein Sci. 7, 1884-1897
24. Bravo-Rodriguez, K., Ismail-Ali, A. F., Klopries, S., Kushnir, S., Ismail, S., Fansa, E. K., Wittinghofer, A., Schulz, F., and Sanchez-Garcia, E. (2014) Predicted incorporation of non-native substrates by a polyketide synthase yields bioactive natural product derivatives ChemBioChem 15, 1991-1997
25. Dunn, B. J., Cane, D. E., and Khosla, C. (2013) Mechanism and specificity of an acyltransferase domain from a modular polyketide synthase Biochemistry 52, 1839-1841
26. Dunn, B. J. and Khosla, C. (2013) Engineering the acyltransferase substrate specificity of assembly line polyketide synthases J. R. Soc. Interface 10, 20130297
27. Dunn, B. J., Watts, K. R., Robbins, T., Cane, D. E., and Khosla, C. (2014) Comparative analysis of the substrate specificity of trans- versus cis-acyltransferases of assembly line polyketide synthases Biochemistry 53, 3796-3806
28. Bonnett, S. A., Rath, C. M., Shareef, A. R., Joels, J. R., Chemler, J. A., Hakansson, K., Reynolds, K., and Sherman, D. H. (2011) Acyl-CoA subunit selectivity in the pikromycin polyketide synthase PikAIV: Steady-state kinetics and active-site occupancy analysis by FTICR-MS Chem. Biol. 18, 1075-1081
29. Babtie, A., Tokuriki, N., and Hollfelder, F. (2010) What makes an enzyme promiscuous? Curr. Opin. Chem. Biol. 14, 200-207
30. Sundermann, U., Bravo-Rodriguez, K., Klopries, S., Kushnir, S., Gomez, H., Sanchez-Garcia, E., and Schulz, F. (2012) Enzyme-directed mutasynthesis: A combined experimental and theoretical approach to substrate recognition of a polyketide synthase ACS Chem. Biol. 8, 443-450
31. Du, Y., Derewacz, D. K., Deguire, S. M., Teske, J., Ravel, J., Sulikowski, G. A., and Bachmann, B. O. (2011) Biosynthesis of the apoptolidins in Nocardiopsis sp. FU 40 Tetrahedron 67, 6568-6575
32. Klopries, S., Sundermann, U., and Schulz, F. (2013) Quantification of N-acetylcysteamine activated methylmalonate incorporation into polyketide biosynthesis Beilstein J. Org. Chem. 9, 664-674
33. Riener, C. K., Kada, G., and Gruber, H. J. (2002) Quick measurement of protein sulfhydryls with Ellmans reagent and with 4,4′-dithiodipyridine Anal. Bioanal. Chem. 373, 266-276
34. Zhang, A., Amalin, D., Shirali, S., Serrano, M. S., Franqui, R. A., Oliver, J. E., Klun, J. A., Aldrich, J. R., Meyerdirk, D. E., and Lapointe, S. L. (2004) Sex pheromone of the pink hibiscus mealybug, Maconellicoccus hirsutus, contains an unusual cyclobutanoid monoterpene Proc. Natl. Acad. Sci. U.S.A. 101, 9601-9606
35. Moss, S. J., Carletti, I., Olano, C., Sheridan, R. M., Ward, M., Math, V., Nur, E. A. M., Brana, A. F., Zhang, M. Q., Leadlay, P. F., Mendez, C., Salas, J. A., and Wilkinson, B. (2006) Biosynthesis of the angiogenesis inhibitor borrelidin: Directed biosynthesis of novel analogues Chem. Commun. (Camb) 2341-2343
36. Kushnir, S., Sundermann, U., Yahiaoui, S., Brockmeyer, A., Janning, P., and Schulz, F. (2012) Minimally invasive mutagenesis gives rise to a biosynthetic polyketide library Angew. Chem., Int. Ed. Engl. 51, 10664-10669
37. Rangan, V. S. and Smith, S. (1997) Alteration of the substrate specificity of the malonyl-CoA/acetyl-CoA:acyl carrier protein S-acyltransferase domain of the multifunctional fatty acid synthase by mutation of a single arginine residue J. Biol. Chem. 272, 11975-11978
38. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. (2003) A graphical user interface to the CCP4 program suite Acta Crystallogr., Sect. D: Biol. Crystallogr. 59, 1131-1137
39. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132
40. 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
41. Piasecki, S. K., Taylor, C. A., Detelich, J. F., Liu, J., Zheng, J., Komsoukaniants, A., Siegel, D. R., and Keatinge-Clay, A. T. (2011) Employing modular polyketide synthase ketoreductases as biocatalysts in the preparative chemoenzymatic syntheses of diketide chiral building blocks Chem. Biol. 18, 1331-1340