Genetic engineering and heterologous expression of the disorazol biosynthetic gene cluster via Red/ET recombineering

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Tu, Qiang ^a,b   Herrmann, Jennifer ^a   Hu, Shengbiao ^c   Raju, Ritesh ^a,d   Bian, Xiaoying ^b   Zhang, Youming ^b   Müller, Rolf ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b SHANDONG UNIVERSITY   (China)

^c HUNAN NORMAL UNIVERSITY   (China)

^d UNIVERSITY OF WESTERN SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DISORAZOL A; OXAZOLE DERIVATIVE;

BACTERIAL ARTIFICIAL CHROMOSOME; BIOSYNTHESIS; DRUG EFFECTS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETIC RECOMBINATION; GENETICS; HUMAN; METABOLISM; MULTIGENE FAMILY; MUTAGENESIS; MYXOCOCCUS XANTHUS; TUMOR CELL LINE;

BIOSYNTHETIC PATHWAYS; CELL LINE, TUMOR; CHROMOSOMES, ARTIFICIAL, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC ENGINEERING; HUMANS; MULTIGENE FAMILY; MUTAGENESIS; MYXOCOCCUS XANTHUS; OXAZOLES; RECOMBINATION, GENETIC;

EID: 84958214556     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21066     Document Type: Article

References (63)

1. Luo, Y., Cobb, R. E. & Zhao, H. Recent advances in natural product discovery. Curr. Opin. Biotechnol. 30, 230-237 (2014).
2. Wenzel, S. C. & Müller, R. The impact of genomics on the exploitation of the myxobacterial secondary metabolome. Nat. Prod. Rep. 26, 1385-1407 (2009).
3. Schäberle, T. F., Lohr, F., Schmitz, A. & König, G. M. Antibiotics from myxobacteria. Nat. Prod. Rep. 31, 953-972 (2014).
4. Gomes, E. S., Schuch, V. & de Macedo Lemos, E. G. Biotechnology of polyketides: new breath of life for the novel antibiotic genetic pathways discovery through metagenomics. Braz. J. Microbiol. 44, 1007-1034 (2014).
5. Strieker, M., Tanović, A. & Marahiel, M. A. Nonribosomal peptide synthetases: structures and dynamics. Curr. Opin. Struct. Biol. 20, 234-240 (2010).
6. Fischbach, M. A. & Walsh, C. T. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev. 106, 3468-3496 (2006).
7. Ongley, S. E. et al. High titer heterologous production of Lyngbyatoxin in E. coli, a protein kinase C activator from an uncultured marine Cyanobacterium. ACS Chem. Biol. 8, 1888-1893 (2013).
8. 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).
9. Ongley, S. E., Bian, X., Neilan, B. A. & Müller, R. Recent advances in the heterologous expression of microbial natural product biosynthetic pathways. Nat. Prod. Rep. 30, 1121-1138 (2013).
10. Bian, X. et al. Direct cloning, genetic engineering, and heterologous expression of the Syringolin biosynthetic gene cluster in E. coli through Red/ET recombineering. ChemBioChem. 13, 1946-1952 (2012).
11. Larionov, V., Kouprina, N., Solomon, G., Barrett, J. C. & Resnick, M. A. Direct isolation of human BRCA2 gene by transformation-associated recombination in yeast. Proc. Natl. Acad. Sci. USA 94, 7384-7387 (1997).
12. Kouprina, N. et al. Functional copies of a human gene can be directly isolated by transformation-associated recombination cloning with a small 3′ end target sequence. Proc. Natl. Acad. Sci. USA 95, 4469-4474 (1998).
13. Zhang, Y., Buchholz, F., Muyrers, J. P. P. & Stewart, A. F. A new logic for DNA engineering using recombination in Escherichia coli. Nat. Genet. 20, 123-128 (1998).
14. Zhang, Y., Muyrers, J. P. P., Testa, G. & Stewart, A. F. DNA cloning by homologous recombination in Escherichia coli. Nat. Biotechnol. 18, 1314-1317 (2000).
15. Zhang, Y., Muyrers, J. P. P., Rientjes, J. & Stewart, A. F. Phage annealing proteins promote oligonucleotide-directed mutagenesis in Escherichia coli and mouse ES cells. Mol. Biol. 4, 1 (2003).
16. Wenzel, S. C. & Müller, R. Recent developments towards the heterologous expression of complex bacterial natural product biosynthetic pathways. Curr. Opin. Biotechnol. 16,594-606 (2005).
17. 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).
18. Perlova, O. et al. Reconstitution of the myxothiazol biosynthetic gene cluster by Red/ET recombination and heterologous expression in Myxococcus xanthus. Appl. Environ. Microbiol. 72, 7485-7494 (2006).
19. Fu, J. et al. Efficient transfer of two large secondary metabolite pathway gene clusters into heterologous hosts by transposition. Nucleic Acids Res. 36, e113 (2008).
20. Wang, A. et al. High level expression and purification of bioactive human alpha-defensin 5 mature peptide in Pichia pastoris. Appl. Microbiol. Biotechnol. 84, 877-884 (2009).
21. Liao, G. J. et al. Cloning, reassembling and integration of the entire nikkomycin biosynthetic gene cluster into Streptomyces ansochromogenes lead to an improved nikkomycin production. Microb. Cell Fact. 9, 6 (2010).
22. Chai, Y. et al. Heterologous expression and genetic engineering of the tubulysin biosynthetic gene cluster using Red/ET recombineering and inactivation mutagenesis. Chem. Biol. 19, 361-371 (2012).
23. Bian, X., Plaza, A., Zhang, Y. & Müller, R. Luminmycins A-C, cryptic natural products from Photorhabdus luminescens identified by heterologous expression in Escherichia coli. J. Nat. Prod. 75(9), 1652-1655 (2012).
24. Bian, X. et al. Heterologous Production of Glidobactins/Luminmycins in Escherichia coli Nissle Containing the Glidobactin Biosynthetic Gene Cluster from Burkholderia DSM7029. ChemBioChem. 15, 2221-2224 (2014).
25. Yin, J. et al. Direct cloning and heterologous expression of the salinomycin biosynthetic gene cluster from Streptomyces albus DSM41398 in S. coelicolor A3(2). Sci. Rep. 5, 15081 (2015).
26. Kolinko, I. et al. Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nat. Nanotech. 9, 193-197 (2014).
27. Weissman, K. J. & Müller, R. Myxobacterial secondary metabolites: bioactivities and modes-of-action. Nat. Prod. Rep. 27, 1276-1295 (2010).
28. Jansen, R., Irschik, H., Reichenbach, H., Wray, V. & Höfle, G. Disorazols: highly cytotoxic metabolites from the sorangicin-producing bacterium Sorangium cellulosum, strain So ce12. Liebigs Ann. Chem. 759-773 (1994).
29. 1, a highly effective antimitotic agent acting on tubulin polymerization and inducing apoptosis in mammalian cells. Biochem. Pharmacol. 67, 927-935 (2004).
30. Schäckel, R., Hinkelmann, B., Sasse, F. & Kalesse, M. The synthesis of novel disorazols. Angew. Chem. Int. Ed. 49, 1619-1622 (2010).
31. Lee, C., An, D., Lee, H. & Cho, K. Correlation between Sorangium cellulosum subgroups and their potential for secondary metabolite production. J. Microbiol. Biotechnol. 23, 297-303 (2013).
32. Hopkins, C. D. & Wipf, P. Isolation, biology and chemistry of the disorazols: new anti-cancer macrodiolides. Nat. Prod. Rep. 26, 585-601 (2009).
33. Seitz, S. et al. Triple negative breast cancers express receptors for LHRH and are potential therapeutic targets for cytotoxic LHRH-analogs, AEZS 108 and AEZS 125. BMC Cancer 14, 847 (2014).
34. 1. J. Am. Chem. Soc. 126, 15346-15347 (2004).
35. 1. BMC Chem. Biol. 10, 1 (2010).
36. 1. J. Pharmacol. Exp. Ther. 332, 906-911 (2010).
37. Kopp, M., Irschik, H., Pradella, S. & Müller, R. Production of the tubulin destabilizer disorazol in Sorangium cellulosum: biosynthetic machinery and regulatory genes. ChemBioChem. 6, 1277-1286 (2005).
38. Carvalho, R. et al. The biosynthetic genes for disorazols, potent cytotoxic compounds that disrupt microtubule formation. Gene 359, 91-98 (2005).
39. Stevens, D. C., Hari, T. P. A. & Boddy, C. N. The role of transcription in heterologous expression of polyketides in bacterial hosts. Nat. Prod. Rep. 30, 1391-1411 (2013).
40. Kang, Y. et al. Knock-out and pull-out recombineering protocols for naturally transformable Burkholderia thailandensis and Burkholderia pseudomallei. Nat. Protoc. 6, 1085-1104 (2011).
41. Fu, J. et al. Full-length RecE enhances linear-linear homologous recombination and facilitates direct cloning for bioprospecting. Nat. Biotech. 30, 440-446 (2012).
42. Julien, B. & Fehd, R. Development of a mariner-based transposon for use in Sorangium cellulosum. Appl. Environ. Microbiol. 69(10), 6299-6301 (2003).
43. Kopp, M. et al. Critical variations of conjugational DNA transfer into secondary metabolite multiproducing Sorangium cellulosum strains So ce12 and So ce56: development of a mariner-based transposon mutagenesis system. J. Biotechnol. 107, 29-40 (2004).
44. 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).
45. Krug, D. & Müller, R. Secondary metabolomics: the impact of mass spectrometry-based approaches on the discovery and characterization of microbial natural products. Nat. Prod. Rep. 31, 768-783 (2014).
46. Moat, A. G., Foster, J. W. & Spector, M. P. Microbial Physiology, 4th ed. (New York, Wiley-Liss, Inc. Pub) (2003).
47. Trun, N. & Trempy, J. Fundamental bacterial genetics. (Malden, MA: Blackwell Pub.) (2004).
48. Irschik, H., Jansen, R., Gerth, K., Höfle, G. & Reichenbach, H. Disorazol A, an efficient inhibitor of eukaryotic organisms isolated from myxobacteria. J. Antibiot. 48, 31-35 (1995).
49. Hearn, B. R. et al. Methanolysis products of disorazol A1 . J. Nat. Prod. 69, 148-150 (2006).
50. Wong, F. T., Jin, X., Mathews, I. I., Cane, D. E. & Khosla, C. Structure and mechanism of the trans-acting acyltransferase from the disorazol synthase. Biochemistry. 50, 6539-6548 (2012).
51. Piel, J. Metabolites from symbiotic bacteria. Nat. Prod. Rep. 26, 338-362 (2009).
52. Till, M. & Race, P. R. Progress challenges and opportunities for the re-engineering of trans-AT polyketide synthases. Biotechnol. Lett. 36, 877-888 (2014).
53. Jensen, P. R. & Hammer, K. The sequence of spacers between the consensus sequences modulates the strength of prokaryotic promoters. Appl. Environ. Microbiol. 64, 82-87 (1998).
54. 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).
55. Richter, C. D., Nietlispach, D., Broadhurst, R. W. & Weissman, K. J. Multienzyme docking in hybrid megasynthetases. Nat. Chem. Biol. 4, 75-81 (2008).
56. Meiser, P. & Müller, R. Two functionally redundant Sfp-type 4-phosphopantetheinyl transferases differentially activate biosynthetic pathways in Myxococcus xanthus. ChemBioChem. 9, 1549-1553 (2008).
57. Buntin, K. et al. Biosynthesis of thuggacins in myxobacteria: comparative cluster analysis reveals basis for natural product structural diversity. Chem. Biol. 17, 342-356 (2010).
58. Piel, J. Biosynthesis of polyketides by trans-AT polyketide synthases. Nat. Prod. Rep. 27, 996-1047 (2010).
59. Dunn, B. J., Watts, K. R., Robbins, T., Cane, D. E. & Khosla, C. Comparative analysis of the substrate specificity of trans- versus cis-acyltransferases of assembly line polyketide synthases. Biochemistry. 53, pp3796-3806 (2014).
60. Lopanik, N. B. et al. 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 (2008).
61. Jensen, K. et al. Polyketide proofreading by an acyltransferase- like enzyme. Chem. Biol. 19, 329-339 (2012).
62. Fu, J., Teucher, M., Anastassiadis, K., Skarnes, W. & Stewart, A. F. A recombineering pipeline to make conditional targeting constructs. Meth. Enzymol. 477, 125-144 (2010).
63. Meiser, P., Bode, H. B. & Müller, R. The unique DKxanthene secondary metabolite family from the myxobacterium Myxococcus xanthus is required for developmental sporulation. Proc. Natl. Acad. Sci. USA 103, 19128-19133 (2006).