Poly specific trans -Acyltransferase machinery revealed via engineered acyl-coa synthetases

ACS Chemical Biology

Volumn 8, Issue 1, 2013, Pages 200-208

  Koryakina, Irina ^a   McArthur, John ^a   Randall, Shan ^a   Draelos, Matthew M ^a   Musiol, Ewa M ^b   Muddiman, David C ^a   Weber, Tilmann ^b   Williams, Gavin J ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ENZYME VARIANT; LONG CHAIN FATTY ACID COENZYME A LIGASE; MALONYL COENZYME A SYNTHETASE; MUTANT PROTEIN; POLYKETIDE SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ENGINEERING; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SYNTHESIS; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN MODIFICATION; TRANS ISOMER; WILD TYPE;

ACYLTRANSFERASES; BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; COENZYME A LIGASES; CRYSTALLOGRAPHY, X-RAY; GENETIC VARIATION; MODELS, MOLECULAR; SUBSTRATE SPECIFICITY;

EID: 84872518753     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb3003489     Document Type: Article

References (38)

1. Staunton, J. and Weissman, K. J. (2001) Polyketide biosynthesis: a millennium review Nat. Prod. Rep. 18, 380-416 (Pubitemid 32773840)
2. Weissman, K. J. and Leadlay, P. F. (2005) Combinatorial biosynthesis of reduced polyketides Nat. Rev. Microbiol. 3, 925-936 (Pubitemid 43078156)
3. Butler, M. S. (2008) Natural products to drugs: natural product-derived compounds in clinical trials Nat. Prod. Rep. 25, 475-516 (Pubitemid 351725315)
4. Hertweck, C. (2009) The biosynthetic logic of polyketide diversity Angew. Chem., Int. Ed. 48, 4688-4716
5. Chan, Y. A., Podevels, A. M., Kevany, B. M., and Thomas, M. G. (2009) Biosynthesis of polyketide synthase extender units Nat. Prod. Rep. 26, 90-114
6. Wilson, M. C. and Moore, B. S. (2011) Beyond ethylmalonyl-CoA: The functional role of crotonyl-CoA carboxylase/reductase homologs in expanding polyketide diversity Nat. Prod. Rep. 29, 72-86
7. Wu, K., Chung, L., Revill, W. P., Katz, L., and Reeves, C. D. (2000) The FK520 gene cluster of Streptomyces hygroscopicus var. ascomyceticus (ATCC 14891) contains genes for biosynthesis of unusual polyketide extender units Gene 251, 81-90 (Pubitemid 30339418)
8. Chan, Y. A., Boyne, M. T., 2nd, Podevels, A. M., Klimowicz, A. K., Handelsman, J., Kelleher, N. L., and Thomas, M. G. (2006) Hydroxymalonyl-acyl carrier protein (ACP) and aminomalonyl-ACP are two additional type I polyketide synthase extender units Proc. Natl. Acad. Sci. U.S.A. 103, 14349-14354 (Pubitemid 44484753)
9. Mo, S., Kim, D. H., Lee, J. H., Park, J. W., Basnet, D. B., Ban, Y. H., Yoo, Y. J., Chen, S. W., Park, S. R., Choi, E. A., Kim, E., Jin, Y. Y., Lee, S. K., Park, J. Y., Liu, Y., Lee, M. O., Lee, K. S., Kim, S. J., Kim, D., Park, B. C., Lee, S. G., Kwon, H. J., Suh, J. W., Moore, B. S., Lim, S. K., and Yoon, Y. J. (2011) Biosynthesis of the allylmalonyl-CoA extender unit for the FK506 polyketide synthase proceeds through a dedicated polyketide synthase and facilitates the mutasynthesis of analogues J. Am. Chem. Soc. 133, 976-985
10. Eustaquio, A. S., McGlinchey, R. P., Liu, Y., Hazzard, C., Beer, L. L., Florova, G., Alhamadsheh, M. M., Lechner, A., Kale, A. J., Kobayashi, Y., Reynolds, K. A., and Moore, B. S. (2009) Biosynthesis of the salinosporamide A polyketide synthase substrate chloroethylmalonyl-coenzyme A from S-adenosyl-L-methionine Proc. Natl. Acad. Sci. U.S.A. 106, 12295-12300
11. Liu, Y., Hazzard, C., Eustaquio, A. S., Reynolds, K. A., and Moore, B. S. (2009) Biosynthesis of salinosporamides from alpha,beta-unsaturated fatty acids: implications for extending polyketide synthase diversity J. Am. Chem. Soc. 131, 10376-10377
12. Wilson, M. C., Nam, S. J., Gulder, T. A., Kauffman, C. A., Jensen, P. R., Fenical, W., and Moore, B. S. (2011) Structure and biosynthesis of the marine streptomycete Ansamycin ansalactam a and its distinctive branched chain polyketide extender unit J. Am. Chem. Soc. 133, 1971-1977
13. Macherla, V. R., Mitchell, S. S., Manam, R. R., Reed, K. A., Chao, T. H., Nicholson, B., Deyanat-Yazdi, G., Mai, B., Jensen, P. R., Fenical, W. F., Neuteboom, S. T., Lam, K. S., Palladino, M. A., and Potts, B. C. (2005) Structure-activity relationship studies of salinosporamide A (NPI-0052), a novel marine derived proteasome inhibitor J. Med. Chem. 48, 3684-3687 (Pubitemid 40776841)
14. 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-M Chem. Biol. 18, 1075-1081
15. Pohl, N. L., Hans, M., Lee, H. Y., Kim, Y. S., Cane, D. E., and Khosla, C. (2001) Remarkably broad substrate tolerance of malonyl-CoA synthetase, an enzyme capable of intracellular synthesis of polyketide precursors J. Am. Chem. Soc. 123, 5822-5823 (Pubitemid 32904726)
16. Chen, A. Y., Schnarr, N. A., Kim, C. Y., Cane, D. E., and Khosla, C. (2006) Extender unit and acyl carrier protein specificity of ketosynthase domains of the 6-deoxyerythronolide B synthase J. Am. Chem. Soc. 128, 3067-3074
17. Hughes, A. J. and Keatinge-Clay, A. (2011) Enzymatic extender unit generation for in vitro polyketide synthase reactions: structural and functional showcasing of Streptomyces coelicolor MatB Chem. Biol. 18, 165-176
18. Koryakina, I. and Williams, G. J. (2011) Mutant malonyl-CoA synthetases with altered specificity for polyketide synthase extender unit generation ChemBioChem 12, 2289-2293
19. Nguyen, T., Ishida, K., Jenke-Kodama, H., Dittmann, E., Gurgui, C., Hochmuth, T., Taudien, S., Platzer, M., Hertweck, C., and Piel, J. (2008) Exploiting the mosaic structure of trans-acyltransferase polyketide synthases for natural product discovery and pathway dissection Nat. Biotechnol. 26, 225-233 (Pubitemid 351225955)
20. Kumar, P., Koppisch, A. T., Cane, D. E., and Khosla, C. (2003) Enhancing the modularity of the modular polyketide synthases: transacylation in modular polyketide synthases catalyzed by malonyl-CoA:ACP transacylase J. Am. Chem. Soc. 125, 14307-14312 (Pubitemid 37452369)
21. Koppisch, A. T. and Khosla, C. (2003) Structure-based mutagenesis of the Malonyl-CoA: Acyl carrier protein transacylase from Streptomyces coelicolor Biochemistry 42, 11057-11064 (Pubitemid 37174398)
22. Keatinge-Clay, A. T., Shelat, A. A., Savage, D. F., Tsai, S. C., Miercke, L. J., O'Connell, J. D., 3rd, Khosla, C., and Stroud, R. M. (2003) Catalysis, specificity, and ACP docking site of Streptomyces coelicolor malonyl-CoA:ACP transacylase Structure 11, 147-154 (Pubitemid 36187417)
23. Cheng, Y. Q., Coughlin, J. M., Lim, S. K., and Shen, B. (2009) Type I polyketide synthases that require discrete acyltransferases Methods Enzymol. 459, 165-186
24. Cheng, Y. Q., Tang, G. L., and Shen, B. (2003) Type I polyketide synthase requiring a discrete acyltransferase for polyketide biosynthesis Proc. Natl. Acad. Sci. U.S.A. 100, 3149-3154 (Pubitemid 36356554)
25. Musiol, E. M., Hartner, T., Kulik, A., Moldenhauer, J., Piel, J., Wohlleben, W., and Weber, T. (2011) Supramolecular templating in kirromycin biosynthesis: the acyltransferase KirCII loads ethylmalonyl-CoA extender onto a specific ACP of the trans-AT PKS Chem. Biol. 18, 438-444
26. Lopanik, N. B., Shields, J. A., Buchholz, T. J., Rath, C. M., Hothersall, J., Haygood, M. G., Hakansson, K., Thomas, C. M., and Sherman, D. H. (2008) In vivo and in vitro trans-acylation by BryP, the putative bryostatin pathway acyltransferase derived from an uncultured marine symbiont Chem. Biol. 15, 1175-1186
27. Wong, F. T., Chen, A. Y., Cane, D. E., and Khosla, C. (2010) Protein-protein recognition between acyltransferases and acyl carrier proteins in multimodular polyketide synthases Biochemistry 49, 95-102
28. Menche, D., Arikan, F., Perlova, O., Horstmann, N., Ahlbrecht, W., Wenzel, S. C., Jansen, R., Irschik, H., and Muller, R. (2008) Stereochemical determination and complex biosynthetic assembly of etnangien, a highly potent RNA polymerase inhibitor from the myxobacterium Sorangium cellulosum J. Am. Chem. Soc. 130, 14234-14243
29. Omura, S., Takeshima, H., Nakagawa, A., Miyazawa, J., Piriou, F., and Lukacs, G. (1977) Studies on the biosynthesis of 16-membered macrolide antibiotics using carbon-13 nuclear magnetic resonance spectroscopy Biochemistry 16, 2860-2866 (Pubitemid 8185677)
30. Inoue, A., Deguchi, T., Yoshida, M., and Shirahata, K. (1983) Biosynthesis and the metabolic-fate of C-14-labeled spiramycin-1 J. Antibiot. 36, 442-444
31. Kakavas, S. J., Katz, L., and Stassi, D. (1997) Identification and characterization of the niddamycin polyketide synthase genes from Streptomyces caelestis J. Bacteriol. 179, 7515-7522 (Pubitemid 27509991)
32. Jackowski, S. and Rock, C. O. (1996) Escherichia coli and Salmonella typhimurium, in Cell. Mol. Biol. (Neidhart, F. C., Ed.), pp 687-694, American Society of Microbiology, Washington, DC.
33. Clarke, K. M., Mercer, A. C., La Clair, J. J., and Burkart, M. D. (2005) In vivo reporter labeling of proteins via metabolic delivery of coenzyme A analogues J. Am. Chem. Soc. 127, 11234-11235 (Pubitemid 41176871)
34. Go, M. K., Chow, J. Y., Cheung, V. W. N., Lim, Y. P., and Yew, W. S. (2012) Establishing a toolkit for precursor-directed polyketide biosynthesis: Exploring substrate promiscuities of acid-CoA ligases Biochemistry 51, 4568-4579
35. Andrews, G. L., Shuford, C. M., Burnett, J. C., Jr., Hawkridge, A. M., and Muddiman, D. C. (2009) Coupling of a vented column with splitless nanoRPLC-ESI-MS for the improved separation and detection of brain natriuretic peptide-32 and its proteolytic peptides J. Chromatogr. B. Analyt. Technol. Biomed. Life. Sci. 877, 948-954
36. Senko, M., Beu, S., and McLafferty, F. (1995) Determination of monoisotopic masses and ion populations for large biomolecules from resolved isotopic distributions J. Am. Soc. Mass Spectrom. 6, 229-233
37. Nepomuceno, A. I., Mason, C. J., Muddiman, D. C., Bergen, H. R., 3rd, and Zeldenrust, S. R. (2004) Detection of genetic variants of transthyretin by liquid chromatography-dual electrospray ionization fourier-transform ion-cyclotron-resonance mass spectrometry Clin. Chem. 50, 1535-1543 (Pubitemid 39121221)
38. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources Nucleic Acids Res. 37, D387-392