Cloning, characterization and heterologous expression of the indolocarbazole biosynthetic gene cluster from marine-derived Streptomyces sanyensis FMA

Marine Drugs

Volumn 11, Issue 2, 2013, Pages 466-488

  Li, Tong ^a   Du, Yuanyuan ^a   Cui, Qiu ^b   Zhang, Jingtao ^b   Zhu, Weiming ^a   Hong, Kui ^c   Li, Wenli ^a  

^a OCEAN UNIVERSITY OF CHINA   (China)

^b QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

^c WUHAN UNIVERSITY   (China)

Author keywords

Biosynthesis; Heterologous expression; Indolocarbazole (ICZ); Streptomyces sanyensis FMA

Indexed keywords

CARBAZOLE DERIVATIVE; INDOLOCARBAZOLE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DNA DETERMINATION; DNA METHYLATION; GENE; GENE CLUSTER; GENE IDENTIFICATION; GENE INACTIVATION; GENE ISOLATION; GENE SEQUENCE; GLYCOSYLATION; HETEROLOGOUS EXPRESSION; ICZ GENE; MARINE BACTERIUM; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SPC GENE; STREPTOMYCES; STREPTOMYCES SANYENSIS;

EID: 84875798079     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md11020466     Document Type: Article

References (41)

1. Omura, S.; Iwai, Y.; Hirano, A.; Nakagawa, A.; Awaya, J.; Tsuchya, H.; Takahashi, Y.; Masuma, R. A new alkaloid AM-2282 of Streptomyces. origin. Taxonomy, fermentation, isolation and preliminary characterization. J. Antibiot. (Tokyo) 1977, 30, 275-282.
2. Sanchez, C.; Mendez, C.; Salas, J.A. Indolocarbazole natural products: Occurrence, biosynthesis, and biological activity. Nat. Prod. Rep. 2006, 23, 1007-1045.
3. Reyes, F.; Fernandez, R.; Rodriguez, A.; Bueno, S.; de Eguilior, C.; Francesch, A.; Cuevas, C. Cytotoxic staurosporines from the marine ascidian Cystodytes solitus. J. Nat. Prod. 2008, 71, 1046-1048.
4. Fu, P.; Yang, C.; Wang, Y.; Liu, P.; Ma, Y.; Xu, L.; Su, M.; Hong, K.; Zhu, W. Streptocarbazoles A and B, two novel indolocarbazoles from the marine-derived actinomycete strain Streptomyces sp. FMA. Org. Lett. 2012, 14, 2422-2425.
5. Acero, N.; Brana, M.F.; Anorbe, L.; Dominguez, G.; Munoz-Mingarro, D.; Mitjans, F.; Piulats, J. Synthesis and biological evaluation of novel indolocarbazoles with anti-angiogenic activity. Eur. J. Med. Chem. 2012, 48, 108-113.
6. Liu, J.; Hu, Y.; Waller, D.L.; Wang, J.; Liu, Q. Natural products as kinase inhibitors. Nat. Prod. Rep. 2012, 29, 392-403.
7. Prudhomme, M. Biological targets of antitumor indolocarbazoles bearing a sugar moiety. Curr. Med. Chem. Anticancer Agents 2004, 4, 509-521.
8. Kurosu, M.; Begari, E. Bacterial protein kinase inhibitors. Drug Dev. Res. 2010, 71, 168-187.
9. Gani, O.A.; Engh, R.A. Protein kinase inhibition of clinically important staurosporine analogues. Nat. Prod. Rep. 2010, 27, 489-498.
10. ClinicalTrials.gov. Available online: http://www.clinicaltrials.gov/ (accessed on 21 November 2012).
11. Onaka, H.; Taniguchi, S.; Igarashi, Y.; Furumai, T. Cloning of the staurosporine biosynthetic gene cluster from Streptomyces sp. TP-A0274 and its heterologous expression in Streptomyces lividans. J. Antibiot. (Tokyo) 2002, 55, 1063-1071.
12. Sanchez, C.; Butovich, I.A.; Brana, A.F.; Rohr, J.; Mendez, C.; Salas, J.A. The biosynthetic gene cluster for the antitumor rebeccamycin: Characterization and generation of indolocarbazole derivatives. Chem. Biol. 2002, 9, 519-531.
13. Kim, S.Y.; Park, J.S.; Chae, C.S.; Hyun, C.G.; Choi, B.W.; Shin, J.; Oh, K.B. Genetic organization of the biosynthetic gene cluster for the indolocarbazole K-252a in Nonomuraea longicatena JCM 11136. Appl. Microbiol. Biotechnol. 2007, 75, 1119-1126.
14. Chiu, H.T.; Chen, Y.L.; Chen, C.Y.; Jin, C.; Lee, M.N.; Lin, Y.C. Molecular cloning, sequence analysis and functional characterization of the gene cluster for biosynthesis of K-252a and its analogs. Mol. Biosyst. 2009, 5, 1180-1191.
15. Gao, Q.; Zhang, C.; Blanchard, S.; Thorson, J.S. Deciphering indolocarbazole and enediyne aminodideoxypentose biosynthesis through comparative genomics: Insights from the AT2433 biosynthetic locus. Chem. Biol. 2006, 13, 733-743.
16. Howard-Jones, A.R.; Walsh, C.T. Enzymatic generation of the chromopyrrolic acid scaffold of rebeccamycin by the tandem action of RebO and RebD. Biochemistry 2005, 44, 15652-15663.
17. Onaka, H. Biosynthesis of indolocarbazole and goadsporin, two different heterocyclic antibiotics produced by actinomycetes. Biosci. Biotechnol. Biochem. 2009, 73, 2149-2155.
18. Asamizu, S.; Shiro, Y.; Igarashi, Y.; Nagano, S.; Onaka, H. Characterization and functional modification of StaC and RebC, which are involved in the pyrrole oxidation of indolocarbazole biosynthesis. Biosci. Biotechnol. Biochem. 2011, 75, 2184-2193.
19. Goldman, P.J.; Ryan, K.S.; Hamill, M.J.; Howard-Jones, A.R.; Walsh, C.T.; Elliott, S.J.; Drennan, C.L. An unusual role for a mobile flavin in StaC-like indolocarbazole biosynthetic enzymes. Chem. Biol. 2012, 19, 855-865.
20. Groom, K.; Bhattacharya, A.; Zechel, D.L. Rebeccamycin and staurosporine biosynthesis: Insight into the mechanisms of the flavin-dependent monooxygenases RebC and StaC. ChemBioChem 2011, 12, 396-400.
21. Ryan, K.S.; Drennan, C.L. Divergent pathways in the biosynthesis of bisindole natural products. Chem. Biol. 2009, 16, 351-364.
22. Sanchez, C.; Zhu, L.; Brana, A.F.; Salas, A.P.; Rohr, J.; Mendez, C.; Salas, J.A. Combinatorial biosynthesis of antitumor indolocarbazole compounds. Proc. Natl. Acad. Sci. USA 2005, 102, 461-466.
23. Howard-Jones, A.R.; Walsh, C.T. Staurosporine and rebeccamycin aglycones are assembled by the oxidative action of StaP, StaC, and RebC on chromopyrrolic acid. J. Am. Chem. Soc. 2006, 128, 12289-12298.
24. Makino, M.; Sugimoto, H.; Shiro, Y.; Asamizu, S.; Onaka, H.; Nagano, S. Crystal structures and catalytic mechanism of cytochrome P450 StaP that produces the indolocarbazole skeleton. Proc. Natl. Acad. Sci. USA 2007, 104, 11591-11596.
25. Olano, C.; Mendez, C.; Salas, J.A. Antitumor compounds from marine actinomycetes. Mar. Drugs 2009, 7, 210-248.
26. Hernandez, L.M.; Blanco, J.A.; Baz, J.P.; Puentes, J.L.; Millan, F.R.; Vazquez, F.E.; Fernandez-Chimeno, R.I.; Gravalos, D.G. 4′-N-methyl- 5′-hydroxystaurosporine and 5′-hydroxystaurosporine, new indolocarbazole alkaloids from a marine Micromonospora sp. strain. J. Antibiot. (Tokyo) 2000, 53, 895-902.
27. Liu, R.; Zhu, T.; Li, D.; Gu, J.; Xia, W.; Fang, Y.; Liu, H.; Zhu, W.; Gu, Q. Two indolocarbazole alkaloids with apoptosis activity from a marine-derived actinomycete Z(2)039-2. Arch. Pharm. Res. 2007, 30, 270-274.
28. Sui, J.L.; Xu, X.X.; Qu, Z.; Wang, H.L.; Lin, H.P.; Xie, Q.Y.; Ruan, J.S.; Hong, K. Streptomyces sanyensis sp. nov., isolated from mangrove sediment. Int. J. Syst. Evol. Microbiol. 2010, 61, 1632-1637.
29. Kui, H. Wuhan University, Wuhan, China. Unpublished work, 2012.
30. Meksuriyen, D.; Cordell, G.A. Biosynthesis of staurosporine, 1. 1H- and 13C-NMR assignments. J. Nat. Prod. 1988, 51, 884-892.
31. Onaka, H. Biosynthesis of heterocyclic antibiotics in actinomycetes and an approach to synthesize the natural compounds. Actinomycetologica 2006, 20, 62-71.
32. Sambrook, J.; Fritsch, E.F.; Maniatis, T. Molecular Cloning: A Laboratory Manual, 2nd ed.; Cold Spring Harbor Laboratory: Cold Spring Harbor, NY, USA, 1989.
33. Paget, M.S.; Chamberlin, L.; Atrih, A.; Foster, S.J.; Buttner, M.J. Evidence that the extracytoplasmic function sigma factor σE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 1999, 181, 204-211.
34. Gust, B.; Challis, G.L.; Fowler, K.; Kieser, T.; Chater, K.F. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. USA 2003, 100, 1541-1546.
35. Gust, B.; Chandra, G.; Jakimowicz, D.; Yuqing, T.; Bruton, C.J.; Chater, K.F. Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv. Appl. Microbiol. 2004, 54, 107-128.
36. Kieser, T.; Bib, M.J.; Buttner, M.J.; Chater, K.F.; Hopwood, D.A. Practical Streptomyces Genetics; The John Innes Foundation: Norwich, UK, 2000.
37. Ishikawa, J.; Hotta, K. FramePlot: A new implementation of the frame analysis for predicting protein-coding regions in bacterial DNA with a high G + C content. FEMS Microbiol. Lett. 1999, 174, 251-253.
38. Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403-410.
39. Datsenko, K.A.; Wanner, B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 2000, 97, 6640-6645.
40. MacNeil, D.J.; Gewain, K.M.; Ruby, C.L.; Dezeny, G.; Gibbons, P.H.; MacNeil, T. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 1992, 111, 61-68.
41. Zhang, Y.; Huang, H.; Chen, Q.; Luo, M.; Sun, A.; Song, Y.; Ma, J.; Ju, J. South Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China. Unpublished work, 2013