Identification and characterization of the biosynthetic gene cluster of thiolutin, a tumor angiogenesis inhibitor, in Saccharothrix algeriensis NRRL B-24137

Anti-Cancer Agents in Medicinal Chemistry

Volumn 15, Issue 3, 2015, Pages 277-284

  Huang, Sheng ^a   Tong, Ming Him ^b   Qin, Zhiwei ^b   Deng, Zixin ^a   Deng, Hai ^b   Yu, Yi ^a  

^a WUHAN UNIVERSITY   (China)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Biosynthesis; Dithiolopyrrolone; Heterologous expression; Saccharothrix algeriensis; Thiolutin

Indexed keywords

METHYLTRANSFERASE; THIOLUTIN; 2 PYRROLIDONE DERIVATIVE; ANGIOGENESIS INHIBITOR; BIOLOGICAL PRODUCT;

ARTICLE; BACTERIAL GENE; BIOINFORMATICS; DNA METHYLATION; ENZYME PURIFICATION; GENE CLUSTER; GENE CONSTRUCT; GENE IDENTIFICATION; GENE LIBRARY; GENETIC SCREENING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOBACTERIUM HALOTOLERANS; POLYMERASE CHAIN REACTION; PSEUDOALTEROMONAS; SACCHAROTHRIX ALGERIENSIS NRRL B 24137; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STREPTOMYCES CLAVULIGERUS; YERSINIA RUCKERI; ACTINOMYCETALES; BIOLOGY; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MULTIGENE FAMILY;

ACTINOMYCETALES; ANGIOGENESIS INHIBITORS; BIOLOGICAL PRODUCTS; BIOSYNTHETIC PATHWAYS; COMPUTATIONAL BIOLOGY; MOLECULAR STRUCTURE; MULTIGENE FAMILY; PYRROLIDINONES;

EID: 84930913335     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/1871520614666141027145200     Document Type: Article

References (35)

1. Liras, P. Holomycin, a dithiolopyrrolone compound produced by Streptomyces clavuligerus. Appl. Microbiol. Biotechnol., 2014, 98(3), 1023-1030.
2. Li, B.; Wever, W. J.; Walsh, C. T.; Bowers, A. A. Dithiolopyrrolones: Biosynthesis, synthesis, and activity of a unique class of disulfidecontaining antibiotics. Nat. Prod. Rep., 2014, 31(7), 905-923.
3. Qin, Z.; Huang, S.; Yu, Y.; Deng, H. Dithiolopyrrolone natural products: Isolation, synthesis and biosynthesis. Mar. Drugs, 2013, 11(10), 3970-3997.
4. Shiozawa, H.; Kagasaki, T.; Kinoshita, T.; Haruyama, H.; Domon, H.; Utsui, Y.; Kodama, K.; Takahashi, S. Thiomarinol, a new hybrid antimicrobial antibiotic produced by a marine bacterium. Fermentation, isolation, structure, and antimicrobial activity. J. Antibiot., 1993, 46(12), 1834-1842.
5. Umezawa, H.; Maeda, K.; Kosaka, H. Isolation of a new antibiotic substance, aureothricin from a strain of Streptomyces. Jpn. Med. J., 1948, 1, 512-517.
6. Li, B.; Lyle, M. P.; Chen, G.; Li, J.; Hu, K.; Tang, L.; Alaoui-Jamali, M. A.; Webster, J. Substituted 6-amino-4H-[1, 2]dithiolo [4, 3-b]pyrrol-5-ones: Synthesis, structure-activity relationships, and cytotoxic activity on selected human cancer cell lines. Bioorg. Med. Chem., 2007, 15(13), 4601-4608.
7. Merrouche, R.; Bouras, N.; Coppel, Y.; Mathieu, F.; Sabaou, N.; Lebrihi, A. New dithiolopyrrolone antibiotics induced by adding sorbic acid to the culture medium of Saccharothrix algeriensis NRRL B-24137. FEMS Microbiol. Lett., 2011, 318(1), 41-46.
8. Oliva, B.; O'Neill, A.; Wilson, J. M.; O'Hanlon, P. J.; Chopra, I. Antimicrobial properties and mode of action of the pyrrothine holomycin. Antimicrob. Agents Chemother., 2001, 45(2), 532-539.
9. Webster, J. M.; Li, J.; Chen, G. Anticancer properties of dithiolopyrrolones. U. S. Patent 6, 020, 360, 2000.
10. Minamiguchi, K.; Kumagai, H.; Masuda, T.; Kawada, M.; Ishizuka, M.; Takeuchi, T. Thiolutin, an inhibitor of HUVEC adhesion to vitronectin, reduces paxillin in HUVECs and suppresses tumor cellinduced angiogenesis. Int. J. Cancer, 2001, 93(3), 307-316.
11. Jia, Y.; Wu, S. L.; Isenberg, J. S.; Dai, S.; Sipes, J. M.; Field, L.; Zeng, B.; Bandle, R. W.; Ridnour, L. A.; Wink, D. A.; Ramchandran, R.; Karger, B. L.; Roberts, D. D. Thiolutin inhibits endothelial cell adhesion by perturbing Hsp27 interactions with components of the actin and intermediate filament cytoskeleton. Cell Stress Chaperones, 2010, 15(2), 165-181.
12. Dai, S.; Jia, Y.; Wu, S. L.; Isenberg, J. S.; Ridnour, L. A.; Bandle, R. W.; Wink, D. A.; Roberts, D. D.; Karger, B. L. Comprehensive characterization of heat shock protein 27 phosphorylation in human endothelial cells stimulated by the microbial dithiole thiolutin. J. Proteome Res., 2008, 7(10), 4384-4395.
13. McConnell, J. R.; McAlpine, S. R. Heat shock proteins 27, 40, and 70 as combinational and dual therapeutic cancer targets. Bioorg. Med. Chem. Lett., 2013, 23(7), 1923-1928.
14. Li, B.; Walsh, C. T. Identification of the gene cluster for the dithiolopyrrolone antibiotic holomycin in Streptomyces clavuligerus. Proc. Nati. Acad. Sci. USA, 2010, 107(46), 19731-19735.
15. Li, B.; Walsh, C. T. Streptomyces clavuligerus HlmI is an intramolecular disulfide-forming dithiol oxidase in holomycin biosynthesis. Biochemistry, 2011, 50(21), 4615-4622.
16. Qin, Z.; Baker, A. T.; Raab, A.; Huang, S.; Wang, T.; Yu, Y.; Jaspars, M.; Secombes, C. J.; Deng, H. The fish pathogen Yersinia ruckeri produces holomycin and uses an RNA methyltransferase for self-resistance. J. Biol. Chem., 2013, 288(21), 14688-14697.
17. Fukuda, D.; Haines, A. S.; Song, Z.; Murphy, A. C.; Hothersall, J.; Stephens, E. R.; Gurney, R.; Cox, R. J.; Crosby, J.; Willis, C. L.; Simpson, T. J.; Thomas, C. M. A natural plasmid uniquely encodes two biosynthetic pathways creating a potent anti-MRSA antibiotic. PloS one, 2011, 6(3), e18031.
18. Lamari, L.; Zitouni, A.; Boudjella, H.; Badji, B.; Sabaou, N.; Lebrihi, A.; Lefebvre, G.; Seguin, E.; Tillequin, F. New dithiolopyrrolone antibiotics from Saccharothrix sp. SA 233. I. Taxonomy, fermentation, isolation and biological activities. J. Antibiot., 2002, 55(8), 696-701.
19. Lamari, L.; Zitouni, A.; Dob, T.; Sabaou, N.; Lebrihi, A.; Germain, P.; Seguin, E.; Tillequin, F. New dithiolopyrrolone antibiotics from Saccharothrix sp. SA 233. II. Physicochemical properties and structure elucidation. J. Antibiot., 2002, 55(8), 702-706.
20. Bouras, N.; Mathieu, F.; Sabaou, N.; Lebrihi, A. Effect of amino acids containing sulfur on dithiolopyrrolone antibiotic productions by Saccharothrix algeriensis NRRL B-24137. J. Appl. Microbiol., 2006, 100(2), 390-397.
21. Bouras, N.; Mathieu, F.; Sabaou, N.; Lebrihi, A. Influence on dithiolopyrrolone antibiotic production by organic acids in Saccharothrix algeriensis NRRL B-24137. Proc. Biochem., 2007, 42, 925-933.
22. Bouras, N.; Merrouche, R.; Lamari, L.; Mathieu, F.; Sabaou, N.; Lebrihi, A. Precursor-directed biosynthesis of new dithiolopyrrolone analogs by Saccharothrix algeriensis NRRL B-24137. Process Biochem., 2008, 43(11), 1244-1252.
23. Bouras, N.; Mathieu, F.; Sabaou, N.; Lebrihi, A. Nutritional requirements for the production of dithiolopyrrolone antibiotics by Saccharothrix algeriensis NRRL B-24137. Enzyme Microb. Tech., 2006, 39(7), 1423-1429.
24. Merrouche, R.; Bouras, N.; Coppel, Y.; Mathieu, F.; Monje, M. C.; Sabaou, N.; Lebrihi, A. Dithiolopyrrolone antibiotic formation induced by adding valeric acid to the culture broth of Saccharothrix algeriensis. J. Nat. Prod., 2010, 73(6), 1164-1166.
25. Chorin, A. C.; Bijeire, L.; Monje, M. C.; Baziard, G.; Lebrihi, A.; Mathieu, F. Expression of pyrrothine N-acyltransferase activities in Saccharothrix algeriensis NRRL B-24137: New insights into dithiolopyrrolone antibiotic biosynthetic pathway. J. Appl. Microbiol., 2009, 107(5), 1751-1762.
26. Saker, S.; Almousa Almaksour, Z.; Chorin, A. C.; Lebrihi, A.; Mathieu, F. Enzymatic synthesis of dithiolopyrrolone antibiotics using cell-free extract of Saccharothrix algeriensis NRRL B-24137 and biochemical characterization of two pyrrothine Nacyltransferases in this extract. J. Microbiol. Biotechnol., 2014, 24(1), 26-35.
27. Saker, S.; Lebrihi, A.; Mathieu, F. Identification of two putative acyltransferase genes potentially implicated in dithiolopyrrolone biosyntheses in Saccharothrix algeriensis NRRL B-24137. Appl. Biochem. Biotechnol., 2014, 173(3), 787-802.
28. Huang, S.; Zhao, Y. D.; Qin, Z. W.; Wang, X. L.; Onega, M.; Chen, L.; He, J.; Yu, Y.; Deng, H. Identification and heterologous expression of the biosynthetic gene cluster for holomycin produced by Streptomyces clavuligerus. Proc. Biochem., 2011, 46(3), 811-816.
29. Overbeek, R.; Olson, R.; Pusch, G. D.; Olsen, G. J.; Davis, J. J.; Disz, T.; Edwards, R. A.; Gerdes, S.; Parrello, B.; Shukla, M.; Vonstein, V.; Wattam, A. R.; Xia, F. F.; Stevens, R. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic. Acids Res., 2014, 42, 206-214.
30. Li, B.; Forseth, R. R.; Bowers, A. A.; Schroeder, F. C.; Walsh, C. T. A backup plan for self-protection: S-methylation of holomycin biosynthetic intermediates in Streptomyces clavuligerus. Chembiochemistry, 2012, 13(17), 2521-2526.
31. Scharf, D. H.; Habel, A.; Heinekamp, T.; Brakhage, A. A.; Hertweck, C. Opposed effects of enzymatic gliotoxin N-and smethylations. J. Am. Chem. Soc., 2014, 136(33), 11674-11679.
32. Awakawa, T.; Zhang, L.; Wakimoto, T.; Hoshino, S.; Mori, T.; Ito, T.; Ishikawa, J.; Tanner, M. E.; Abe, I. A methyltransferase initiates terpene cyclization in teleocidin B biosynthesis. J. Am. Chem. Soc., 2014, 136(28), 9910-9913.
33. Wu, Y.; Kang, Q.; Shang, G.; Spiteller, P.; Carroll, B.; Yu, T. W.; Su, W.; Bai, L.; Floss, H. G. N-methylation of the amide bond by methyltransferase asm10 in ansamitocin biosynthesis. Chembiochemistry, 2011, 12(11), 1759-1766.
34. Giessen, T. W.; Von Tesmar, A. M.; Marahiel, M. A. Insights into the generation of structural diversity in a tRNA-dependent pathway for highly modified bioactive cyclic dipeptides. Chem. Biol., 2013, 20(6), 828-838.
35. Chatterjee, J.; Gilon, C.; Hoffman, A.; Kessler, H. N-methylation of peptides: A new perspective in medicinal chemistry. Accounts Chem. Res., 2008, 41(10), 1331-1342.