Mining and engineering natural-product biosynthetic pathways

Nature Chemical Biology

Volumn 3, Issue 7, 2007, Pages 379-386

  Wilkinson, Barrie ^a   Micklefield, Jason ^b  

^a BIOTICA TECHNOLOGY LTD   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID SYNTHASE; NATURAL PRODUCT; PEPTIDE SYNTHASE; POLYKETIDE SYNTHASE;

BIODIVERSITY; CHEMICAL GENETICS; COMBINATORIAL CHEMISTRY; GENE CLUSTER; GENE LIBRARY; HETEROLOGOUS EXPRESSION; HIGH THROUGHPUT SCREENING; MOLECULAR CLONING; PHARMACOGENOMICS; PRIORITY JOURNAL; REVIEW;

EID: 34250701119     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2007.7     Document Type: Review

References (67)

1. Newman, D.J., Cragg, G.M. & Snader, K.M. Natural products as a source of new drugs over the period 1981-2002. J. Nat. Prod. 66, 1002-1037 (2003).
2. Spring, D.R. Chemical genetics to chemical genomics: small molecules offer big insights. Chem. Soc. Rev. 34, 472-482 (2005).
3. Koehn, F.E. & Carter, G.T. The evolving role of natural products in drug discovery. Nature Rev. Drug Discov. 4, 206-220 (2005).
4. Wilkinson, B. & Bachmann, B.O. Biocatalysis in pharmaceutical preparation and alteration. Curr. Opin. Chem. Biol. 10, 169-176 (2006).
5. Ro, D.-K. et al. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440, 940-943 (2006).
6. Wang, J. et al. Platensimycin is a selective FabF inhibitor with potent antibiotic properties. Nature 441, 358-361 (2006).
7. Bentley, S.D. et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141-147 (2002).
8. Oliynyk, M. et al. Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL2338. Nat. Biotechnol. 25, 447-453 (2007).
9. Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380 (2005).
10. Ostash, B.B., Saghatelian, A. & Walker, S. A streamlined metabolic pathway for the biosynthesis of moenomycin A. Chem. Biol. 14, 257-267 (2007).
11. Song, L. et al. Type III polyketide synthase β-ketoacyl-ACP starter unit and ethylmalonyl-CoA extender unit selectivity discovered by Streptomyces coelicolor genome mining. J. Am. Chem. Soc. 128, 14754-14755 (2006).
12. McAlpine, J.B. et al. Microbial genomics as a guide to drug discovery and structural elucidation: ECO-02301, a novel antifungal agent, as an example. J. Nat. Prod. 68, 493-496 (2005).
13. Lautru, S., Deeth, R.J., Bailey, L.M. & Challis, G.L. Discovery of a new peptide product by Streptomyces coelicolor genome mining. Nat. Chem. Biol. 1, 265-269 (2005).
14. Zazopoulos, E. et al. A genomics-guided approach for discovering and expressing cryptic metabolic pathways. Nat. Biotechnol. 21, 187-190 (2003).
15. Bachmann, B.O., McAlpine, J.B., Zazopolous, E., Farnet, C.M. & Piraee, M. Farnesyl dibenzodiazopines, their production with microorganisms, and their use as antitumor, antibacterial and antiinflammatory agents. Patent Cooperation Treaty patent WO2004065591 (2004).
16. Bergmann, S. et al. Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat. Chem. Biol. 3, 213-217 (2007).
17. Camilli, A. & Bassler, B.L. Bacterial small-molecule signalling pathways. Science 311, 1113-1116 (2006).
18. Amann, R.I., Ludwig, W. & Schleifer, K.-H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143-169 (1995).
19. Brady, S.F. & Clardy, J. Palmitoylputrescine, an antibiotic isolated from the heterologous expression of DNA extracted from bromeliad tank water. J. Nat. Prod. 67, 1283-1286 (2004).
20. Brady, S.F. & Clardy, J. Cloning and heterologous expression of isocyanide biosynthetic genes from environmental DNA. Angew. Chem. Int. Ed. Engl. 44, 7063-7065 (2005).
21. Pfeifer, B.A., Admiraal, S.J., Gramajo, H., Cane, D.E. & Khosla, C. Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science 291, 1790-1792 (2001).
22. Watanabe, K. et al. Total biosynthesis of antitumor nonribosomal peptides in Escherichia coli. Nat. Chem. Biol. 2, 423-428 (2006).
23. Schmidt, E.W. et al. Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc. Natl. Acad. Sci. USA 102, 7315-7320 (2005).
24. Long, P.F., Dunlap, W.C., Battershill, C.N. & Jaspars, M. Shotgun cloning and heterologous expression of the patellamide gene cluster as a strategy to achieved sustained metabolite production. ChemBioChem 6, 1760-1765 (2005).
25. Wenzel, S.C. et al. Heterologous expression of a myxobacterial natural products assembly line in Pseudomonads via Red/ET recombineering. Chem. Biol. 12, 349-356 (2005).
26. Gross, F. et al. Metabolic engineering of Pseudomonas putida for methylmalonyl-CoA biosynthesis to enable complex heterologous secondary metabolite formation. Chem. Biol. 13, 1253-1264 (2006).
27. Richardson, S.M., Wheelan, S.J., Yarrington, R.M. & Boeke, J.D. GeneDesign: rapid, automated design of multikilobase synthetic genes. Genome Res. 16, 550-556 (2006).
28. Kodumal, S.J. et al. Total synthesis of long DNA sequences: synthesis of a contiguous 32-kb polyketide synthase gene cluster. Proc. Natl. Acad. Sci. USA 101, 15573-15578 (2004).
29. Menzella, H.G. et al. Combinatorial polyketide biosynthesis by de novo design and rearrangement of modular polyketide synthase genes. Nat. Biotechnol. 23, 1171-1176 (2005).
30. Moss, S.J., Martin, C.J. & Wilkinson, B. Loss of co-linearity by modular polyketide synthases: a mechanism for the evolution of chemical diversity. Nat. Prod. Rep. 21, 575-593 (2004).
31. Heathcote, M.L., Staunton, J. & Leadlay, P.F. Role of type II thioesterases: evidence for removal of short acyl chains produced by aberrant decarboxylation of chain extender units. Chem. Biol. 8, 207-220 (2001).
32. Yeh, E., Kohli, R.M., Bruner, S.D. & Walsh, C.T. Type II thioesterase restores activity of a NRPS module stalled with an aminoacyl-S-enzyme that cannot be elongated. ChemBioChem 5, 1290-1293 (2004).
33. Uguru, G.C. et al. Active-site modifications of adenylation domains lead to hydrolysis of upstream nonribosomal peptidyl thioester intermediates. J. Am. Chem. Soc. 126, 5032-5033 (2004).
34. Arnold, F.H. Fancy footwork in the sequence-space shuffle. Nat. Biotechnol. 24, 328-330 (2006).
35. Yoshikuni, Y., Ferrin, T.E. & Keasling, J.D. Designed divergent evolution of enzyme function. Nature 440, 1078-1082 (2006).
36. Stachelhaus, T., Schneider, A. & Maraheil, M.A. Rational design of peptide antibiotics by targeted replacement of bacterial and fungal domains. Science 269, 69-72 (1995).
37. Cortés, J. et al. Repositioning of a domain in a modular polyketide synthase to promote specific chain length cleavage. Science 268, 1487-1489 (1995).
38. Donadio, S., Staver, M.J., McAlpine, J.B., Swanson, S.J. & Katz, L. Modular organization of genes required for complex polyketide biosynthesis. Science 252, 675-679 (1991).
39. Maier, T., Jenni, S. & Ban, N. Architecture of a mammalian fatty acid synthase at 4.5Å resolution. Science 311, 1258-1262 (2006).
40. Jenni, S., Leibundgut, M., Maier, T. & Ban, N. Architecture of a fungal fatty acid synthase at 5 Å resolution. Science 311, 1263-1267 (2006).
41. Tang, Y., Kim, C.-Y., Mathews, I.I., Cane, D.E. & Khosla, C. 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 (2006).
42. Jenni, S., Leibundgut, M., Boehringer, D., Frick, C. & Ban, N. Structural basis for substrate delivery by acyl carrier protein in the yeast fatty acid synthase. Science 316, 288-290 (2007).
43. Weissman, K.J. The structural basis for docking in modular polyketide biosynthesis. ChemBioChem 7, 485-494 (2006).
44. Hahn, M. & Stachelhaus, T. Harnessing the potential of communication-mediating domains for the biocombinatorial synthesis of nonribosomal peptides. Proc. Natl. Acad. Sci. USA 103, 275-280 (2006).
45. Koglin, A. et al. Conformational switches modulate protein interactions in peptide antibiotic synthetases. Science 312, 273-276 (2006).
46. Qiao, C., Wilson, D.J., Bennett, E.M. & Aldrich, C.C. A Mechanism-based aryl carrier protein/thiolation domain affinity probe. J. Am. Chem Soc. 129, 6350-6351 (2007).
47. Worthington, A.S., Rivera, H., Jr., Torpey, J.W., Alexander, M.D. & Burkart, M.D. Mechanism-based protein cross-linking probes to investigate carrier protein-mediated biosynthesis. ACS Chem. Biol. 1, 687-691 (2006).
48. Miao, V. et al. Genetic engineering in Streptomyces roseosporus to produce hybrid lipopeptide antibiotics. Chem. Biol. 13, 269-276 (2006).
49. Nguyen, K.T. et al. Combinatorial biosynthesis of novel antibiotics related to daptomycin. Proc. Natl. Acad. Sci. USA 103, 17462-17467 (2006).
50. Kopp, F., Grünewald, J., Mahlert, C. & Marahiel, M.A. Chemoenzymatic design of acidic lipopeptide hybrids: new insights into the structure-activity relationship of daptomycin and A54145. Biochemistry 45, 10474-10481 (2006).
51. Wilcoxen, K.M., Leman, L.J., Weinberger, D.A., Huang, Z-Z. & Ghadiri, M.R. Biomimetic catalysis of intermodular aminoacyl transfer. J. Am. Chem. Soc. 129, 748-749 (2007).
52. Leman, L.J., Weinberger, D.A., Huang, Z.-Z., Wilcoxen, K.M. & Ghadiri, M.R. Functional and mechanistic analyses of biomimetic aminoacyl transfer reactions in de novo designed coiled coil peptides via rational active site engineering. J. Am. Chem. Soc. 129, 2959-2966 (2007).
53. Chan, Y.A. et al. Hydroxymalonyl-acyl carrier protein (ACP) and aminomalonyl-ACP are two additional type I polyketide synthase extender units. Proc. Natl. Acad. Sci. USA 103, 14349-14354 (2006).
54. Reeves, C.D. et al. Alteration of the substrate specificity of a modular polyketide synthase acyltransferase domain through site-directed mutagenesis. Biochemistry 40, 15464-15470 (2001).
55. Del Vecchio, F. et al. Active-site residue, domain and module swaps in modular polyketide synthases. J. Ind. Microbiol. Biotechnol. 30, 489-494 (2003).
56. Baerga-Ortiz, A. et al. Directed mutagenesis alters the stereochemistry of catalysis by isolated ketoreductase domains from the erythromycin polyketide synthase. Chem. Biol. 13, 277-285 (2006).
57. Weist, S. & Sussmuth, R.D. Mutational biosynthesis - a tool for the generation of structural diversity in the biosynthesis of antibiotics. Appl. Microbiol. Biotechnol. 68, 141-150 (2005).
58. Weissman, K.J. Mutasynthesis - uniting chemistry and genetics for drug discovery. Trends Biotechnol. 25, 139-142 (2007).
59. Li, S.M. & Heide, L. New aminocoumarin antibiotics from genetically engineered Streptomyces strains. Curr. Med. Chem. 12, 419-427 (2005).
60. Thibodeaux, C.J., Melancon, C.E. & Liu, H-W. Unusual sugar biosynthesis and natural product glycodiversification. Nature 446, 1008-1016 (2007).
61. Rodriguez, L. et al. Engineering deoxysugar biosynthetic pathways from antibiotic-producing microorganisms, a tool to produce novel glycosylated bioactive compounds. Chem. Biol. 9, 721-729 (2002).
62. Hoffmeister, D. et al. Engineered urdamycin glycosyltransferases are broadened and altered in substrate specificity. Chem. Biol. 9, 287-295 (2002).
63. Zhang, C. et al. Exploiting the reversibility of natural product glycosyltransferase-catalyzed reactions. Science 313, 1291-1294 (2006).
64. McCoy, E. & O'Connor, S.E. Directed biosynthesis of alkaloid analogs in the medicinal plant Catharanthus roseus. J. Am. Chem. Soc. 128, 14276-14277 (2006).
65. Chen, S., Galan, M.C., Coltharp, C. & O'Connor, S.E. Redesign of a central enzyme in alkaloid biosynthesis. Chem. Biol. 13, 1137-1141 (2006).
66. Zhang, Y. et al. Using unnatural protein fusions to engineer resveratrol biosynthesis in yeast and mammalian cells. J. Am. Chem. Soc. 128, 13030-13031 (2006).
67. Breinbauer, R., Vetter, I.R. & Waldmann, H. From protein domains to drug candidates - natural products as guiding principles in the design and synthesis of compound libraries. Angew. Chem. Int. Ed. 41, 2879-2890 (2002).