Autonomous folding of interdomain regions of a modular polyketide synthase

FEBS Journal

Volumn 274, Issue 9, 2007, Pages 2196-2209

  Richter, Carsten D ^a   Stanmore, David A ^a   Miguel, Ricardo N ^a   Moncrieffe, Martin C ^a   Tran, Lucky ^a   Brewerton, Suzanne ^a,c   Meersman, Filip ^a,d   Broadhurst, R William ^a   Weissman, Kira J ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SAARLAND UNIVERSITY   (Germany)

^c Astex   (United Kingdom)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Genetic engineering; Interdomain linker; Modular polyketide synthase; Multienzyme; Polyketide biosynthesis

Indexed keywords

DIMER; ERYTHROMYCIN SYNTHASE; POLYKETIDE SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; ENZYME STRUCTURE; GEL FILTRATION; MODEL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; ULTRACENTRIFUGATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CLONING, MOLECULAR; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYKETIDE SYNTHASES; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN;

ANIMALIA; SUS;

EID: 34247326876     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05757.x     Document Type: Article

References (54)

1. Staunton J Weissman K J (2001) Polyketide biosynthesis: a millennium review. Nat Prod Rep 18, 380 416.
2. Weissman KJ Leadlay PF (2005) Combinatorial biosynthesis of reduced polyketides. Nat Rev Microbiol 3, 925 936.
3. Hill AM (2006) The biosynthesis, molecular genetics and enzymology of the polyketide-derived metabolites. Nat Prod Rep 23, 256 320.
4. Smith S, Witkowski A Joshi AK (2003) Structural and functional organization of the animal fatty acid synthase. Prog Lipid Res 42, 289 317.
5. Udwary DW, Merski M Townsend CA (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.
6. Bedford D, Jacobsen JR, Luo G, Cane DE Khosla C (1996) A functional chimeric modular polyketide synthase generated via domain replacement. Chem Biol 3, 827 831.
7. McDaniel R, Thamchaipenet A, Gustafsson C, Fu H, Betlach M Ashley G (1999) Multiple genetic modifications of the erythromycin polyketide synthase to produce a library of novel 'unnatural' natural products. Proc Natl Acad Sci USA 96, 1846 1851.
8. Patel K, Piagentini M, Rascher A, Tian ZQ, Buchanan GO, Regentin R, Hu Z, Hutchinson CR McDaniel R (2004) Engineered biosynthesis of geldanamycin analogs for Hsp90 inhibition. Chem Biol 11, 1625 1633.
9. Wilkinson CJ, Frost EJ, Staunton J Leadlay PF (2001) Chain initiation on the soraphen-producing modular polyketide synthase from Sorangium cellulosum. Chem Biol 8, 1197 1208.
10. Hans M, Hornung A, Dziarnowski A, Cane DE Khosla C (2003) Mechanistic analysis of acyl transferase domain exchange in polyketide synthase modules. J Am Chem Soc 125, 5366 5374.
11. Ruan X, Pereda A, Stassi DL, Zeidner D, Summers RG, Jackson M, Shivakumar A, Kakavas S, Staver MJ, Donadio S et al. (1997) Acyltransferase domain substitutions in erythromycin polyketide synthase yield novel erythromycin derivatives. J Bacteriol 179, 6416 6425.
12. Petkovič H, Lill RE, Sheridan RM, Wilkinson B, McCormick EL, McArthur HA, Staunton J, Leadlay PF Kendrew SG (2003) A novel erythromycin, 6-desmethyl erythromycin D, made by substituting an acyltransferase domain of the erythromycin polyketide synthase. J Antibiot 56, 543 551.
13. Reeves CD, Murli S, Ashley GW, Piagentini M, Hutchinson CR McDaniel R (2001) Alteration of the substrate specificity of a modular polyketide synthase acyltransferase domain through site-specific mutations. Biochemistry 40, 15464 15470.
14. Aparicio JF, Caffrey P, Marsden AF, Staunton J Leadlay PF (1994) Limited proteolysis and active-site studies of the first multienzyme component of the erythromycin-producing polyketide synthase. J Biol Chem 269, 8524 8528.
15. Hong H, Appleyard AN, Siskos AP, Garcia-Bernardo J, Staunton J Leadlay PF (2004) Chain initiation on type I modular polyketide synthases revealed by limited proteolysis and ion-trap mass spectrometry. FEBS J 272, 2373 2387.
16. Kim CY, Alekseyev VY, Chen AY, Tang Y, Cane DE Khosla C (2004) Reconstituting modular activity from separated domains of 6-deoxyerythronolide B synthase. Biochemistry 43, 13892 13898.
17. Maier T, Jenni S Ban N (2006) Architecture of mammalian fatty acid synthase at 4.5 Å resolution. Science 311, 1258 1262.
18. Chirala SS, Huang WY, Jayakumar A, Sakai K Wakil SJ (1997) Animal fatty acid synthase: functional mapping and cloning and expression of the domain I constituent activities. Proc Natl Acad Sci USA 94, 5588 5593.
19. Chirala SS, Jayakumar A, Gu ZW Wakil SJ (2001) Human fatty acid synthase: role of interdomain in the formation of catalytically active synthase dimer. Proc Natl Acad Sci USA 98, 3104 3108.
20. Witkowski A, Joshi AK Smith S (2004) Characterization of the β-carbon processing reactions of the mammalian cytosolic fatty acid synthase: role of the central core. Biochemistry 43, 10458 10466.
21. Keatinge-Clay AT Stroud RM (2006) The structure of a ketoreductase determines the organization of the β-carbon processing enzymes of modular polyketide synthases. Structure 14, 737 748.
22. Ansari MZ, Yadav G, Gokhale RS Mohanty D (2004) NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res 32, W405 W413.
23. Tang Y, Kim CY, Mathews II, Cane DE 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 USA 103, 11124 11129.
24. Tollinger M, Konrat R, Hilbert BH, Marsh EN Kräutler B (1998) How a protein prepares for B12 binding: structure and dynamics of the B12-binding subunit of glutamate mutase from Clostridium tetanomorphum. Structure 6, 1021 1033.
25. Hoffman B, Konrat R, Bothe H, Buckel W Kräutler B (1999) Structure and dynamics of the B12-binding subunit of glutamate mutase from Clostridium cochlearium. Eur J Biochem 263, 178 188.
26. Mancia F, Smith GA Evans PR (1999) Crystal structure of substrate complexes of methylmalonyl-CoA mutase. Biochemistry 38, 7999 8005.
27. Drennan CL, Huang S, Drummond JT, Matthews RG Ludwig ML (1994) How a protein binds B12: a 3.0 Å X-ray structure of B12-binding domains of methionine synthase. Science 266, 1669 1674.
28. Rangan VS, Joshi AK Smith S (1998) Fatty acid synthase dimers containing catalytically active β-ketoacyl synthase or malonyl/acetyltransferase domains in only one subunit can support fatty acid synthesis at the acyl carrier protein domains of both subunits. J Biol Chem 273, 34949 34953.
29. Shi J, Blundell TL Mizuguchi K (2001) fugue: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310, 243 257.
30. Sreerama N, Venyaminov SY Woody RW (2000) Estimation of protein secondary structure from CD spectra: inclusion of denatured proteins with native protein in the analysis. Anal Biochem 287, 243 251.
31. Whitmore L Wallace BA (2004) dichroweb, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32, W668 W673.
32. Kabsch W Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577 2637.
33. Laskowski RA, MacArthur MW, Moss DS Thornton JM (1993) procheck: a program to check the stereochemical quality of protein structures. J Appl Cryst 26, 283 291.
34. Tang G-L, Cheng Y-Q Shen B (2004) Leinamycin biosynthesis revealing unprecedented architectural complexity for a hybrid polyketide synthase and non-ribosomal peptide synthetase. Chem Biol 11, 33 45.
35. Mochizuki S, Hiratsu K, Suwa M, Ishii T, Sugino F, Yamada K Kinashi H (2003) The large linear plasmid pSLA2-L of Streptomyces rochei has an unusually condensed gene organization for secondary metabolism. Mol Microbiol 48, 1501 1510.
36. Siskos AP, Baerga-Ortiz A, Bali S, Stein V, Mamdani H, Spiteller D, Popovic B, Spencer JB, Staunton J, Weissman KJ et al. (2005) Molecular basis of Celmer's rules: stereochemistry of catalysis by isolated ketoreductase domains from modular polyketide synthases. Chem Biol 12, 1145 1153.
37. Rangan VS, Joshi AK Smith S (2001) Mapping the functional topology of the animal fatty acid synthase by mutant complementation in vitro. Biochemistry 40, 10792 10799.
38. Smith S (2006) Architectural options for a fatty acid synthase. Science 311, 1251 1252.
39. Townsend CA, Crawford JM Bililign T (2006) New images invoke FAScinating questions. Chem Biol 13, 349 351.
40. Gogos A, Mu H Shapiro L (2003) Putative enoyl reductase domain of a polyketide synthase 1PQW. http://www.rcsb.org/pdb/navarsearch.do?newSearch= yes&isAuthorSearch=no&radioset=All&inputQuickSearch=1pqw&image. x=42&image.y=5
41. Sambrook J, Fritsch EF Maniatis T, eds. (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Yadav G, Gokhale RS Mohanty D (2003) Computational approach for prediction of domain organization and substrate specificity of modular polyketide synthases. J Mol Biol 328, 335 363.
43. Thompson JD, Higgins DG Gibson TJ (1994) clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 11, 4673 4680.
44. boxshade. Pretty printing and shading of multiple-alignment files. http://www.ch.embnet.org/software/BOX_form.html
45. Cuff JA, Clamp ME, Siddiqui AS, Finlay M Barton GJ (1998) JPRED: a consensus secondary structure prediction server. Bioinformatics 14, 892 893.
46. Sali A, Potterton L, Yuan F, van Vlijmen H Karplus M (1995) Evaluation of comparative protein modeling by modeller. Proteins 23, 318 326.
47. Eisenberg D, Luthy R Bowie JU (1997) verify3d: assessment of protein models with three-dimensional profiles. Meth Enzymol 277, 396 404.
48. Mizuguchi K, Deane CM, Blundell TL, Johnson MS Overington JP (1998) joy: protein sequence-structure representation and analysis. Bioinformatics 14, 617 623.
49. Jackson M Mantsch HH (1995) The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit Rev Biochem Mol Biol 30, 95 120.
50. Lepre CA, Moore JM Peng JW (2004) Theory and applications of NMR-based screening in pharmaceutical research. Chem Rev 104, 3641 3676.
51. Schuck P Rossmanith P (2000) Determination of the sedimentation coefficient distribution by least-squares boundary modelling. Biopolymers 54, 328 341.
52. Johnson ML, Correia JJ, Yphantis DA Halvorson HR (1981) Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques. Biophys J 36, 575 588.
53. Miguel RN (2004) Sequence patterns derived from the automated prediction of functional residues in structurally-aligned homologous protein families. Bioinformatics 20, 2380 2389.
54. Schuck P (2000) Size distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78, 1606 1619.