Structure and stereospecificity of the dehydratase domain from the terminal module of the rifamycin polyketide synthase

Biochemistry

Volumn 52, Issue 49, 2013, Pages 8916-8928

  Gay, Darren ^a   You, Young Ok ^b   Keatinge Clay, Adrian ^a   Cane, David E ^b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC-RESOLUTION; DIASTEREO-SELECTIVITY; MODEL SUBSTRATES; POLYKETIDE SYNTHASES; REDUCTION PRODUCTS; RESOLUTION STRUCTURE; STEREOSPECIFICITY; SUBSTITUTION PATTERNS;

ANTIBIOTICS; CATALYSIS; DEHYDRATION; STEREOSELECTIVITY;

SUBSTRATES;

2 METHYL 2 PENTENOYL; 2 METHYL 3 HYDROXYACYL; 2 METHYL 3 HYDROXYPENTANOYL; 2 METHYL 3 KETOPENTANOYL; ACYL CARRIER PROTEIN; AMIDE SYNTHASE; CHEMICAL COMPOUND; ERYTHROMYCIN; HYDROLYASE; N ACETYLCYSTEAMINE; OXIDOREDUCTASE; PANTETHEINE THIOESTER DERIVATIVE; POLYKETIDE SYNTHASE; PROTEIN ERYACP6; PROTEIN RIFACP10; PROTEIN RIFDH10; PROTEIN RIFKR10; RIFAMYCIN; THIOESTER; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHEMICAL BOND; CONTROLLED STUDY; DIASTEREOISOMER; HYDRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; STEREOCHEMISTRY; STEREOSPECIFICITY; STRUCTURE ANALYSIS; SUBSTITUTION REACTION;

EID: 84890480085     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400988t     Document Type: Article

References (59)

1. Smith, S. and Tsai, S. C. (2007) The type I fatty acid and polyketide synthases: A tale of two megasynthases Nat. Prod. Rep. 24, 1041-1072
2. Sherman, D. H. and Smith, J. L. (2006) Clearing the skies over modular polyketide synthases ACS Chem. Biol. 1, 505-509
3. Cane, D. E. (2010) Programming of erythromycin biosynthesis by a modular polyketide synthase J. Biol. Chem. 285, 27517-27523
4. Piel, J. (2010) Biosynthesis of polyketides by trans-AT polyketide synthases Nat. Prod. Rep. 27, 996-1047
5. Lewy, D. S., Gauss, C. M., Soenen, D. R., and Boger, D. L. (2002) Fostriecin: Chemistry and biology Curr. Med. Chem. 9, 2005-2032
6. Kong, R., Liu, X., Su, C., Ma, C., Qiu, R., and Tang, L. (2013) Elucidation of the biosynthetic gene cluster and the post-PKS modification mechanism for fostriecin in Streptomyces pulveraceus Chem. Biol. 20, 45-54
7. Palaniappan, N., Alhamadsheh, M. M., and Reynolds, K. A. (2008) cis -Δ(2,3)-double bond of phoslactomycins is generated by a post-PKS tailoring enzyme J. Am. Chem. Soc. 130, 12236-12237
8. Olano, C., Wilkinson, B., Sanchez, C., Moss, S. J., Sheridan, R., Math, V., Weston, A. J., Brana, A. F., Martin, C. J., Oliynyk, M., Mendez, C., Leadlay, P. F., and Salas, J. A. (2004) Biosynthesis of the angiogenesis inhibitor borrelidin by Streptomyces parvulus Tu4055: Cluster analysis and assignment of functions Chem. Biol. 11, 87-97
9. 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
10. Akey, D. L., Razelun, J. R., Tehranisa, J., Sherman, D. H., Gerwick, W. H., and Smith, J. L. (2010) Crystal structures of dehydratase domains from the curacin polyketide biosynthetic pathway Structure 18, 94-105
11. Schupp, T., Toupet, C., Engel, N., and Goff, S. (1998) Cloning and sequence analysis of the putative rifamycin polyketide synthase gene cluster from Amycolatopsis mediterranei FEMS Microbiol. Lett. 159, 201-207
12. August, P. R., Tang, L., Yoon, Y. J., Ning, S., Muller, R., Yu, T. W., Taylor, M., Hoffmann, D., Kim, C. G., Zhang, X., Hutchinson, C. R., and Floss, H. G. (1998) Biosynthesis of the ansamycin antibiotic rifamycin: Deductions from the molecular analysis of the rif biosynthetic gene cluster of Amycolatopsis mediterranei S699 Chem. Biol. 5, 69-79
13. Tang, L., Yoon, Y. J., Choi, C. Y., and Hutchinson, C. R. (1998) Characterization of the enzymatic domains in the modular polyketide synthase involved in rifamycin B biosynthesis by Amycolatopsis mediterranei Gene 216, 255-265
14. Alhamadsheh, M. M., Palaniappan, N., Daschouduri, S., and Reynolds, K. A. (2007) Modular polyketide synthases and cis double bond formation: Establishment of activated cis -3-cyclohexylpropenoic acid as the diketide intermediate in phoslactomycin biosynthesis J. Am. Chem. Soc. 129, 1910-1911
15. Bonnett, S. A., Whicher, J. R., Papireddy, K., Florova, G., Smith, J. L., and Reynolds, K. A. (2013) Structural and stereochemical analysis of a modular polyketide synthase ketoreductase domain required for the generation of a cis -alkene Chem. Biol. 20, 772-783
16. World Health Organization (2010) Standard Treatment Regimens. In Treatment of Tuberculosis Guidelines, 4 th ed., pp 29-30, World Health Organization Press, Geneva.
17. Hertweck, C. (2009) The biosynthetic logic of polyketide diversity Angew. Chem., Int. Ed. 48, 4688-4716
18. Stratmann, A., Toupet, C., Schilling, W., Traber, R., Oberer, L., and Schupp, T. (1999) Intermediates of rifamycin polyketide synthase produced by an Amycolatopsis mediterranei mutant with inactivated rifF gene Microbiology 145, 3365-3375
19. Yu, T.-W., Shen, Y., Doi-Katayama, Y., Tang, L., Park, C., Moore, B. S., Richard Hutchinson, C., and Floss, H. G. (1999) Direct evidence that the rifamycin polyketide synthase assembles polyketide chains processively Proc. Natl. Acad. Sci. U.S.A. 96, 9051-9056
20. Floss, H. G. and Yu, T. W. (1999) Lessons from the rifamycin biosynthetic gene cluster Curr. Opin. Chem. Biol. 3, 592-597
21. Keatinge-Clay, A. (2008) Crystal structure of the erythromycin polyketide synthase dehydratase J. Mol. Biol. 384, 941-953
22. Donadio, S., McAlpine, J. B., Sheldon, P. J., Jackson, M., and Katz, L. (1993) An erythromycin analog produced by reprogramming of polyketide synthesis Proc. Natl. Acad. Sci. U.S.A. 90, 7119-7123
23. Valenzano, C. R., You, Y. O., Garg, A., Keatinge-Clay, A., Khosla, C., and Cane, D. E. (2010) Stereospecificity of the dehydratase domain of the erythromycin polyketide synthase J. Am. Chem. Soc. 132, 14697-14699
24. Reid, R., Piagentini, M., Rodriguez, E., Ashley, G., Viswanathan, N., Carney, J., Santi, D. V., Hutchinson, C. R., and McDaniel, R. (2003) A model of structure and catalysis for ketoreductase domains in modular polyketide synthases Biochemistry 42, 72-79
25. Caffrey, P. (2003) Conserved amino acid residues correlating with ketoreductase stereospecificity in modular polyketide synthases ChemBioChem 4, 654-657
26. Keatinge-Clay, A. T. (2007) A tylosin ketoreductase reveals how chirality is determined in polyketides Chem. Biol. 14, 898-908
27. Castonguay, R., Valenzano, C. R., Chen, A. Y., Keatinge-Clay, A., Khosla, C., and Cane, D. E. (2008) Stereospecificity of ketoreductase domains 1 and 2 of the tylactone modular polyketide synthase J. Am. Chem. Soc. 130, 11598-11599
28. Palaniappan, N., Kim, B. S., Sekiyama, Y., Osada, H., and Reynolds, K. A. (2003) Enhancement and selective production of phoslactomycin B, a protein phosphatase IIa inhibitor, through identification and engineering of the corresponding biosynthetic gene cluster J. Biol. Chem. 278, 35552-35557
29. Tang, L., Ward, S., Chung, L., Carney, J. R., Li, Y., Reid, R., and Katz, L. (2004) Elucidating the mechanism of cis double bond formation in epothilone biosynthesis J. Am. Chem. Soc. 126, 46-47
30. Vergnolle, O., Hahn, F., Baerga-Ortiz, A., Leadlay, P. F., and Andexer, J. N. (2011) Stereoselectivity of isolated dehydratase domains of the borrelidin polyketide synthase: Implications for cis double bond formation ChemBioChem 12, 1011-1014
31. You, Y. O., Khosla, C., and Cane, D. E. (2013) Stereochemistry of reductions catalyzed by methyl-epimerizing ketoreductase domains of polyketide synthases J. Am. Chem. Soc. 135, 7406-7409
32. Guo, X., Liu, T., Valenzano, C. R., Deng, Z., and Cane, D. E. (2010) Mechanism and stereospecificity of a fully saturating polyketide synthase module: Nanchangmycin synthase module 2 and its dehydratase domain J. Am. Chem. Soc. 132, 14694-14696
33. 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
34. 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
35. Kim, C. Y., Alekseyev, V. Y., Chen, A. Y., Tang, Y., Cane, D. E., and Khosla, C. (2004) Reconstituting modular activity from separated domains of 6-deoxyerythronolide B synthase Biochemistry 43, 13892-13898
36. Valenzano, C. R., Lawson, R. J., Chen, A. Y., Khosla, C., and Cane, D. E. (2009) The biochemical basis for stereochemical control in polyketide biosynthesis J. Am. Chem. Soc. 131, 18501-18511
37. Wu, N., Tsuji, S. Y., Cane, D. E., and Khosla, C. (2001) Assessing the balance between protein-protein interactions and enzyme-substrate interactions in the channeling of intermediates between polyketide synthase modules J. Am. Chem. Soc. 123, 6465-6474
38. Haapalainen, A. M., Merilainen, G., Pirila, P. L., Kondo, N., Fukao, T., and Wierenga, R. K. (2007) Crystallographic and kinetic studies of human mitochondrial acetoacetyl-CoA thiolase: The importance of potassium and chloride ions for its structure and function Biochemistry 46, 4305-4321
39. Agnihotri, G. and Liu, H. W. (2003) Enoyl-CoA hydratase. Reaction, mechanism, and inhibition Bioorg. Med. Chem. 11, 9-20
40. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning, A Laboratory Manual, 2 nd ed., Cold Spring Harbor Laboratory Press, Plainview, NY.
41. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
42. De Marco, V., Stier, G., Blandin, S., and de Marco, A. (2004) The solubility and stability of recombinant proteins are increased by their fusion to NusA Biochem. Biophys. Res. Commun. 322, 766-771
43. Weinreb, P. H., Quadri, L. E., Walsh, C. T., and Zuber, P. (1998) Stoichiometry and specificity of in vitro phosphopantetheinylation and aminoacylation of the valine-activating module of surfactin synthetase Biochemistry 37, 1575-1584
44. 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
45. Collaborative Computational Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
46. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
47. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
48. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
49. 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
50. Siskos, A. P., Baerga-Ortiz, A., Bali, S., Stein, V., Mamdani, H., Spiteller, D., Popovic, B., Spencer, J. B., Staunton, J., Weissman, K. J., and Leadlay, P. F. (2005) Molecular basis of Celmer's rules: Stereochemistry of catalysis by isolated ketoreductase domains from modular polyketide synthases Chem. Biol. 12, 1145-1153
51. Bevitt, D. J., Staunton, J., and Leadlay, P. F. (1993) Mutagenesis of the dehydratase active site in the erythromycin-producing polyketide synthase Biochem. Soc. Trans. 21, 30S
52. Pasta, S., Witkowski, A., Joshi, A. K., and Smith, S. (2007) Catalytic residues are shared between two pseudosubunits of the dehydratase domain of the animal fatty acid synthase Chem. Biol. 14, 1377-1385
53. Kimber, M. S., Martin, F., Lu, Y., Houston, S., Vedadi, M., Dharamsi, A., Fiebig, K. M., Schmid, M., and Rock, C. O. (2004) The structure of (3 R)-hydroxyacyl-acyl carrier protein dehydratase (FabZ) from Pseudomonas aeruginosa J. Biol. Chem. 279, 52593-52602
54. Bahnson, B. J. and Anderson, V. E. (1991) Crotonase-catalyzed β-elimination is concerted: A double isotope effect study Biochemistry 30, 5894-5906
55. Sedgwick, B., Morris, C., and French, S. J. (1978) Stereochemical course of dehydration catalyzed by the yeast fatty acid synthetase J. Chem. Soc., Chem. Commun. 193-194
56. Kapur, S., Lowry, B., Yuzawa, S., Kenthirapalan, S., Chen, A. Y., Cane, D. E., and Khosla, C. (2012) Reprogramming a module of the 6-deoxyerythronolide B synthase for iterative chain elongation Proc. Natl. Acad. Sci. U.S.A. 109, 4110-4115
57. Guo, X., Liu, T., Deng, Z., and Cane, D. E. (2012) Essential role of the donor acyl carrier protein in stereoselective chain translocation to a fully reducing module of the nanchangmycin polyketide synthase Biochemistry 51, 879-887
58. Liu, W., Du, L., Zhang, L., Chen, J., Shen, X., and Jiang, H. (2007) Helicobacter pylori acyl carrier protein: Expression, purification, and its interaction with β-hydroxyacyl-ACP dehydratase Protein Expression Purif. 52, 74-81
59. Anand, S. and Mohanty, D. (2012) Modeling holo-ACP:DH and holo-ACP:KR complexes of modular polyketide synthases: A docking and molecular dynamics study BMC Struct. Biol. 12, 10