Examining the role of hydrogen bonding interactions in the substrate specificity for the loading step of polyketide synthase thioesterase domains

Biochemistry

Volumn 47, Issue 45, 2008, Pages 11793-11803

  Wang, Meng ^a   Boddy, Christopher N ^a  

^a SYRACUSE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBONS; BINDING SITES; BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; CARBOHYDRATES; CIRCULAR DICHROISM SPECTROSCOPY; DICHROISM; ENZYMES; FLOW INTERACTIONS; HYDROGEN; HYDROGEN BONDS; HYDROPHOBICITY; NONMETALS; OPTICAL PROPERTIES; ORGANIC COMPOUNDS; PLANTS (BOTANY); POLYMERS;

ACYL CHAINS; BINDING CAVITIES; BIOSYNTHETIC PATHWAYS; CARBOHYDRATE RECOGNITIONS; CIRCULAR DICHROISMS; CONSERVED POLAR RESIDUES; DIFFERENT SUBSTRATES; DO-MAINS; HIGH RESOLUTIONS; HYDROGEN BOND DONORS; HYDROGEN BONDING INTERACTIONS; HYDROGEN BONDINGS; HYDROPHOBIC INTERACTIONS; INACTIVE MUTANTS; LINEAR SUBSTRATES; MACROCYCLIC; MOLECULAR BASES; PICROMYCIN; POLYKETIDE; POLYKETIDE SYNTHASE; POLYKETIDES; RELATIVE MAGNITUDES; SIDE CHAIN HYDROGEN BONDINGS; SINGLE SITES; STRUCTURAL DATUMS; SUBSTRATE SPECIFICITIES; TERTIARY STRUCTURES; THIOESTERASE;

SUBSTRATES;

MACROCYCLIC COMPOUND; MUTANT PROTEIN; PIKROMYCIN; POLYKETIDE; POLYKETIDE SYNTHASE; THIOL ESTER HYDROLASE;

ARTICLE; CIRCULAR DICHROISM; CYCLIZATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; MOLECULAR RECOGNITION; MUTATION; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE;

ESTERASES; HYDROGEN BONDING; MACROLIDES; MOLECULAR STRUCTURE; MULTIENZYME COMPLEXES; MUTAGENESIS, SITE-DIRECTED; POLYKETIDE SYNTHASES; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS);

EID: 55849123035     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800963y     Document Type: Article

References (55)

1. Wiley, P. F., Gerzon, K., Flynn, E. H., Sigal, M. V., Weaver, O., Quarck, U. C., Chauvette, R. R., and Monahan, R. (1957) Erythromycin. X. Structure of Erythromycin. J. Am. Chem. Soc. 79, 6062-6070.
2. Mao, J. C., and Wiegand, R. G. (1968) Mode of action of macrolides. Biochim. Biophys. Acta 157, 404-413.
3. Donadio, S., Staver, M. J., McAlpine, J. B., Swanson, S. J., and Katz, L. (1991) Modular organization of genes required for complex polyketide biosynthesis. Science 252, 675-679.
4. Golding, B. T., and Rickards, R. W. (1966) The structure of the macrolide antibiotic pimaricin. Tetrahedron Lett., 3551-3557.
5. Aparicio, J. F., Fouces, R., Mendes, M. V., Olivera, N., and Martin, J. F. (2000) A complex multienzyme system encoded by five polyketide synthase genes is involved in the biosynthesis of the 26-membered polyene macrolide pimaricin in Streptomyces natalensis. Chem. Biol. 7, 895-905.
6. Gerth, K., Bedorf, N., Hofle, G., Irschik, H., and Reichenbach, H. (1996) Epothilons A and B: Antifungal and cytotoxic compounds from Sorangium cellulosum (Myxobacteria). Production, physicochemical and biological properties. J. Antibiot. 49, 560-563.
7. Tang, L., Shah, S., Chung, L., Carney, J., Katz, L., Khosla, C., and Julien, B. (2000) Cloning and heterologous expression of the epothilone gene cluster. Science 287, 640-642.
8. Molnar, I., Schupp, T., Ono, M., Zirkle, R., Milnamow, M., Nowak-Thompson, B., Engel, N., Toupet, C., Stratmann, A., Cyr, D. D., Gorlach, J., Mayo, J. M., Hu, A., Goff, S., Schmid, J., and Ligon, J. M. (2000) The biosynthetic gene cluster for the microtubule-stabilizing agents epothilones A and B from Sorangium cellulosum So ce90. Chem. Biol. 7, 97-109.
9. Kohli, R. M., and Walsh, C. T. (2003) Enzymology of acyl chain macrocyclization in natural product biosynthesis. Chem. Commun., 297-307.
10. Boddy, C. N., Schneider, T. L., Hotta, K., Walsh, C. T., and Khosla, C. (2003) Epothilone C macrolactonization and hydrolysis are catalyzed by the isolated thioesterase domain of epothilone polyketide synthase. J. Am. Chem. Soc. 125, 3428-3429.
11. He, W. G., Wu, J. Q., Khosla, C., and Cane, D. E. (2006) Macrolactonization to 10-deoxymethynolide catalyzed by the recombinant thioesterase of the picromycin. Bioorg. Med. Chem. Lett. 16, 391-394.
12. Kopp, F., and Marahiel, M. A. (2007) Macrocyclization strategies in polyketide and nonribosomal peptide biosynthesis. Nat. Prod. Rep. 24, 735-749.
13. Aldrich, C. C., Venkatraman, L., Sherman, D. H., and Fecik, R. A. (2005) Chemoenzymatic synthesis of the polyketide macrolactone 10-deoxymethynolide. J. Am. Chem. Soc. 127, 8910-8911.
14. Gokhale, R. S., Hunziker, D., Cane, D. E., and Khosla, C. (1999) Mechanism and specificity of the terminal thioesterase domain from the erythromycin polyketide synthase. Chem. Biol. 6, 117-125.
15. Lu, H. X., Tsai, S. C., Khosla, C., and Cane, D. E. (2002) Expression, site-directed mutagenesis, and steady state kinetic analysis of the terminal thioesterase domain of the methymycin. Biochemistry 41, 12590-12597.
16. Sharma, K. K., and Boddy, C. N. (2007) The thioesterase domain from the pimaricin and erythromycin biosynthetic pathways can catalyze hydrolysis of simple thioester substrates. Bioorg. Med. Chem. Lett. 17, 3034-3037.
17. Weissman, K. J., Smith, C. J., Hanefeld, U., Aggarwal, R., Bycroft, M., Staunton, J., and Leadlay, P. F. (1998) The thioesterase of the erythromycin-producing polyketide synthase: Influence of acyl chain structure on the mode of release of substrate analogues from the acyl enzyme intermediates. Angew. Chem., Int. Ed. 37, 1437-1440.
18. Xue, Q., Ashley, G., Hutchinson, C. R., and Santi, D. V. (1999) A multiplasmid approach to preparing large libraries of polyketides. Proc. Natl. Acad. Sci. U.S.A. 96, 11740-11745.
19. Jacobsen, J. R., Hutchinson, C. R., Cane, D. E., and Khosla, C. (1997) Precursor-directed biosynthesis of erythromycin analogs by an engineered polyketide synthase. Science 277, 367-369.
20. Kao, C. M., McPherson, M., McDaniel, R. N., Fu, H., Cane, D. E., and Khosla, C. (1997) Gain of Function Mutagenesis of the Erythromycin Polyketide Synthase. 2. Engineered Biosynthesis of an Eight-Membered Ring Tetraketide Lactone. J. Am. Chem. Soc. 119, 11339-11340.
21. Kao, C. M., Luo, G. L., Katz, L., Cane, D. E., and Khosla, C. (1995) Manipulation of Macrolide Ring Size by Directed Mutagenesis of a Modular Polyketide Synthase. J. Am. Chem. Soc. 117, 9105-9106.
22. Jacobsen, J. R., Cane, D. E., and Khosla, C. (1998) Spontaneous priming of a downstream module in 6-deoxyerythronolide B synthase leads to polyketide biosynthesis. Biochemistry 37, 4928-4934.
23. Schetter, B., and Mahrwald, R. (2006) Modern aldol methods for the total synthesis of polyketides. Angew. Chem., Int. Ed. 45, 7506-7525.
24. Menzella, H. G., Reid, R., Carney, J. R., Chandran, S. S., Reisinger, S. J., Patel, K. G., Hopwood, D. A., and Santi, D. V. (2005) Combinatorial polyketide biosynthesis by de novo design and rearrangement of modular polyketide synthase genes. Nat. Biotechnol. 23, 1171-1176.
25. Kittendorf, J. D., and Sherman, D. H. (2006) Developing tools for engineering hybrid polyketide synthetic pathways. Curr. Opin. Biotechnol. 17, 597-605.
26. Staunton, J., and Weissman, K. J. (2001) Polyketide biosynthesis: A millennium review. Nat. Prod. Rep. 18, 380-416.
27. Walsh, C. T. (2002) Combinatorial biosynthesis of antibiotics: Challenges and opportunities. ChemBioChem 3, 125-134.
28. Bruner, S. D., Weber, T., Kohli, R. M., Schwarzer, D., Marahiel, M. A., Walsh, C. T., and Stubbs, M. T. (2002) Structural basis for the cyclization of the lipopeptide antibiotic surfactin by the thioesterase domain SrfTE. Structure 10, 301-310.
29. Pemble, C. W., IV, Johnson, L. C., Kridel, S. J., and Lowther, W. T. (2007) Crystal structure of the thioesterase domain of human fatty acid synthase inhibited by Orlistat. Nat. Struct. Mol. Biol. 14, 704-709.
30. Tsai, S. C., Miercke, L. J. W., Krucinski, J., Gokhale, R., Chen, J. C. H., Foster, P. G., Cane, D. E., Khosla, C., and Stroud, R. M. (2001) Crystal structure of the macrocycle-forming thioesterase domain of the erythromycin polyketide synthase: Versatility from a unique substrate channel. Proc. Natl. Acad. Sci. U.S.A. 98, 14808-14813.
31. Tsai, S. C., Lu, H. X., Cane, D. E., Khosla, C., and Stroud, R. M. (2002) Insights into channel architecture and substrate specificity from crystal structures of two macrocycle-forming thioesterases of modular polyketide synthases. Biochemistry 41, 12598-12606.
32. Giraldes, J. W., Akey, D. L., Kittendorf, J. D., Sherman, D. H., Smith, J. L., and Fecik, R. A. (2006) Structural and mechanistic insights into polyketide macrolactonization from polyketide-based affinity labels. Nat. Chem. Biol. 2, 531-536.
33. Akey, D. L., Kittendorf, J. D., Giraldes, J. W., Fecik, R. A., Sherman, D. H., and Smith, J. L. (2006) Structural basis for macrolactonization by the pikromycin thioesterase. Nat. Chem. Biol. 2, 537-542.
34. Qian, Z., Fields, C. J., Yu, Y., and Lutz, S. (2007) Recent progress in engineering α/β hydrolase-fold family members. Biotechnol. J. 2, 192-200.
35. Sambrook, J. F., and Russell, D. W., Eds. (2000) Molecular cloning: A laboratory manual, 3rd ed., Cold Spring Harbor Laboratory Press, Plainview, NY.
36. Kustedjo, K., Deechongkit, S., Kelly, J. W., and Cravatt, B. F. (2003) Recombinant expression, purification, and comparative characterization of torsinA and its torsion dystonia-associated variant ΔE-torsinA. Biochemistry 42, 15333-15341.
37. Koepf, E. K., Petrassi, H. M., Sudol, M., and Kelly, J. W. (1999) WW: An isolated three-stranded antiparallel β-sheet domain that unfolds and refolds reversibly: Evidence for a structured hydrophobic cluster in urea and GdnHCl and a disordered thermal unfolded state. Protein Sci. 8, 841-853.
38. Pazirandeh, M., Chirala, S. S., and Wakil, S. J. (1991) Site-directed mutagenesis studies on the recombinant thioesterase domain of chicken fatty acid synthase expressed in Escherichia coli. J. Biol. Chem. 266, 20946-20952.
39. Witkowski, A., Witkowska, H. E., and Smith, S. (1994) Reengineering the specificity of a serine active-site enzyme. Two active-site mutations convert a hydrolase to a transferase. J. Biol. Chem. 269, 379-383.
40. Li, J., Szittner, R., Derewenda, Z. S., and Meighen, E. A. (1996) Conversion of serine-114 to cysteine-114 and the role of the active site nucleophile in acyl transfer by myristoyl-ACP thioesterase from Vibrio harveyi. Biochemistry 35, 9967-9973.
41. Nardini, M., and Dijkstra, B. W. (1999) α/β hydrolase fold enzymes: The family keeps growing. Curr. Opin. Struct. Biol. 9, 732-737.
42. Fersht, A. (1998) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding, W. H. Freeman, New York.
43. Fasman, G. D., Ed. (1996) Circular Dichroism and the Conformational Analysis of Biomolecules, Plenum Press, New York.
44. Xue, Y., Zhao, L., Liu, H. W., and Sherman, D. H. (1998) A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: Architecture of metabolic diversity. Proc. Natl. Acad. Sci. U.S.A. 95, 12111-12116.
45. 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.
46. 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.
47. Roujeinikova, A., Simon, W. J., Gilroy, J., Rice, D. W., Rafferty, J. B., and Slabas, A. R. (2007) Structural studies of fatty acyl-(acyl carrier protein) thioesters reveal a hydrophobic binding cavity that can expand to fit longer substrates. J. Mol. Biol. 365, 135-145.
48. Leibundgut, M., Jenni, S., Frick, C., and Ban, N. (2007) Structural basis for substrate delivery by acyl carrier protein in the yeast fatty acid synthase. Science 316, 288-290.
49. Tran, L., Tosin, M., Spencer, J. B., Leadlay, P. F., and Weissman, K. J. (2008) Covalent Linkage Mediates Communication between ACP and TE Domains in Modular Polyketide Synthases. ChemBioChem 9, 905-915.
50. Song, F., Zhuang, Z., and Dunaway-Mariano, D. (2007) Structure-activity analysis of base and enzyme-catalyzed 4-hydroxybenzoyl coenzyme A hydrolysis. Bioorg. Chem. 35, 1-10.
51. Stivers, J. T., and Nagarajan, R. (2006) Probing enzyme phosphoester interactions by combining mutagenesis and chemical modification of phosphate ester oxygens. Chem. Rev. 106, 3443-3467.
52. Elgavish, S., and Shaanan, B. (1997) Lectin-carbohydrate interactions: Different folds, common recognition principles. Trends Biochem. Sci. 22, 462-467.
53. Ohtaki, A., Iguchi, A., Mizuno, M., Tonozuka, T., Sakano, Y., and Kamitori, S. (2003) Mutual conversion of substrate specificities of Thermoactinomyces vulgaris R-47 α-amylases TVAI and TVAII by site-directed mutagenesis. Carbohydr. Res. 338, 1553-1558.
54. Wada, M., Hsu, C. C., Franke, D., Mitchell, M., Heine, A., Wilson, I., and Wong, C. H. (2003) Directed evolution of N-acetyl-neuraminic acid aldolase to catalyze enantiomeric aldol reactions. Bioorg. Med. Chem. 11, 2091-2098.
55. Hsu, C. C., Hong, Z., Wada, M., Franke, D., and Wong, C. H. (2005) Directed evolution of D-sialic acid aldolase to L-3- deoxymanno-2-octulosonic acid (L-KDO) aldolase. Proc. Natl. Acad. Sci. U.S.A. 102, 9122-9126.