Collismycin a biosynthesis in Streptomyces sp. CS40 is regulated by iron levels through two pathway-specific regulators

Microbiology (United Kingdom)

Volumn 160, Issue PART 3, 2014, Pages 467-478

  Vior, Natalia M ^a   Olano, Carlos ^a   García, Ignacio ^a   Méndez, Carmen ^a   Salas, José A ^a  

^a DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CLMR1 PROTEIN; CLMR2 PROTEIN; COLLISMYCIN A; IRON; MUTANT PROTEIN; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG;

ANTIBIOTIC BIOSYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENE OVEREXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATOR GENE; SCALE UP; STREPTOMYCES; TRANSCRIPTION REGULATION; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY;

2,2'-DIPYRIDYL; AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; IRON; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; SEQUENCE ALIGNMENT; STREPTOMYCES; TRANSCRIPTION FACTORS;

EID: 84896815796     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.075218-0     Document Type: Article

References (51)

1. Antonini, I., Claudi, F., Cristalli, G., Franchetti, P., Grifantini, M. & Martelli, S. (1981). N*-N*-S* tridentate ligand system as potential antitumor agents. J Med Chem 24, 1181-1184.
2. Bascarán, V., Hardisson, C. & Braña, A. F. (1989). Regulation of nitrogen catabolic enzymes in Streptomyces clavuligerus. J Gen Microbiol 135, 2465-2474.
3. Bérdy, J. (2012). Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65, 385-395.
4. Berntsson, R. P., Smits, S. H., Schmitt, L., Slotboom, D. J. & Poolman, B. (2010). A structural classification of substrate-binding proteins. FEBS Lett 584, 2606-2617.
5. Bibb, M. J. (2005). Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 8, 208-215.
6. Bierman, M., Logan, R., O'Brien, K., Seno, E. T., Rao, R. N. & Schoner, B. E. (1992). Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces sp. Gene 116, 43-49.
7. Chater, K. F. & Chandra, G. (2008). The use of the rare UUA codon to define "expression space" for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces. J Microbiol 46, 1-11.
8. Chen-Roetling, J., Sinanan, J. & Regan, R. F. (2012). Effect of iron chelators on methemoglobin and thrombin preconditioning. Translational Stroke Res 3, 452-459.
9. Cundliffe, E. (2008). Control of tylosin biosynthesis in Streptomyces fradiae. J Microbiol Biotechnol 18, 1485-1491.
10. Deng, W., Li, C. & Xie, J. (2013). The underling mechanism of bacterial TetR/AcrR family transcriptional repressors. Cell Signal 25, 1608-1613.
11. Fernández, E., Weissbach, U., Sánchez Reillo, C., Braña, A. F., Méndez, C., Rohr, J. & Salas, J. A. (1998). Identification of two genes from Streptomyces argillaceus encoding glycosyltransferases involved in transfer of a disaccharide during biosynthesis of the antitumor drug mithramycin. J Bacteriol 180, 4929-4937.
12. Flores, F. J. & Martín, J. F. (2004). Iron-regulatory proteins DmdR1 and DmdR2 of Streptomyces coelicolor form two different DNAprotein complexes with iron boxes. Biochem J 380, 497-503.
13. Flores, F. J., Barreiro, C., Coque, J. J. R. & Martín, J. F. (2005). Functional analysis of two divalent metal-dependent regulatory genes dmdR1 and dmdR2 in Streptomyces coelicolor and proteome changes in deletion mutants. FEBS J 272, 725-735.
14. Funk, A. & Divekar, P. V. (1959). Caerulomycin, a new antibiotic from Streptomyces caeruleus Baldacci. I. Production, isolation, assay, and biological properties. Can J Microbiol 5, 317-321.
15. García, I., Vior, N. M., Braña, A. F., González-Sabin, J., Rohr, J., Moris, F., Méndez, C. & Salas, J. A. (2012). Elucidating the biosynthetic pathway for the polyketide-nonribosomal peptide collismycin A: mechanism for formation of the 2,29-bipyridyl ring. Chem Biol 19, 399-413.
16. García, I., Vior, N. M., González-Sabín, J., Braña, A. F., Rohr, J., Moris, F., Méndez, C. & Salas, J. A. (2013). Engineering the biosynthesis of the polyketide-nonribosomal peptide collismycin A for generation of analogs with neuroprotective activity. Chem Biol 20, 1022-1032.
17. Gómez, C., Horna, D. H., Olano, C., Palomino-Schätzlein, M., Pineda-Lucena, A., Carbajo, R. J., Braña, A. F., Méndez, C. & Salas, J. A. (2011). Amino acid precursor supply in the biosynthesis of the RNA polymerase inhibitor streptolydigin by Streptomyces lydicus. J Bacteriol 193, 4214-4223.
18. Gómez, C., Olano, C., Méndez, C. & Salas, J. A. (2012). Three pathway-specific regulators control streptolydigin biosynthesis in Streptomyces lydicus. Microbiology 158, 2504-2514.
19. Gomi, S., Amano, S., Sato, E., Miyadoh, S. & Kodama, Y. (1994). Novel antibiotics SF2738A, B and C, and their analogs produced by Streptomyces sp. J Antibiot (Tokyo) 47, 1385-1394.
20. Kieser, T., Bibb, M., Chater, K., Butter, M. & Hopwood, D. (2000). Practical Streptomyces Genetics: a Laboratory Manual. Norwich, UK: John Innes Foundation.
21. Li, Q., Wang, X., Bartlett, R., Pinay, G., Kan, D., Zhang, W. & Sun, J. (2012). Ferrous iron phosphorus in sediments: development of a quantification method through 2,29-bipyridine extraction. Water Environ Res 84, 2037-2044.
22. Liu, G., Chater, K. F., Chandra, G., Niu, G. & Tan, H. (2013). Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev 77, 112-143.
23. Locher, K. P. (2009). Structure and mechanism of ATP-binding cassette transporters. Phil Trans R Soc B 364, 239-245.
24. Martinez Gil, A., Egea, P. U., Medina Padilla, M., García Palomero, E., Pérez Baz, J., Fernández Chimeno, R. I., Medarde Fernández, A., Canedo Hernández, L. M., Romero Millán, F. & other authors (2008). Use of collismycin and derivatives thereof as oxidative stress inhibitors. US Patent WO2007/017146.
25. McInnes, A. G., Smith, D. G., Wright, J. L. C. & Vining, L. C. (1977). Caerulomycins B and C, new 2,29-dipyridyl derivatives from Streptomyces caeruleus. Can J Chem 55, 4159-4165.
26. McInnes, A. G., Smith, D. G., Walter, J. A., Wright, J. L. C., Vining, L. C. & Arsenault, G. P. (1978). Caerulomycin D, a novel glycosidic derivative of 3,4-dihydroxy-2,29-dipyridyl 6-aldoxime from Streptomyces caeruleus. Can J Chem 56, 1836-1842.
27. Miethke, M. & Marahiel, M. A. (2007). Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71, 413-451.
28. Nakouti, I., Sihanonth, P. & Hobbs, G. (2012). A new approach to isolating siderophore-producing actinobacteria. Lett Appl Microbiol 55, 68-72.
29. Nett, M., Ikeda, H. & Moore, B. S. (2009). Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26, 1362-1384.
30. Nocentini, G. & Barzi, A. (1996). The 2,29-bipyridyl-6-carbothioamide copper (II) complex differs from the iron (II) complex in its biochemical effects in tumor cells, suggesting possible differences in the mechanism leading to cytotoxicity. Biochem Pharmacol 52, 65-71.
31. Nocentini, G. & Barzi, A. (1997). Antitumor activity of 2,29-bipyridyl-6-carbothioamide: a ribonucleotide reductase inhibitor. Gen Pharmacol 29, 701-706.
32. Olano, C., Méndez, C. & Salas, J. A. (2011). Molecular insights on the biosynthesis of antitumour compounds by actinomycetes. Microb Biotechnol 4, 144-164.
33. Oldham, M. L., Davidson, A. L. & Chen, J. (2008). Structural insights into ABC transporter mechanism. Curr Opin Struct Biol 18, 726-733.
34. Peláez, A., Ribas-Aparicio, R., Gómez, A. & Rodicio, M. (2001). Structural and functional characterization of the recR gene of Streptomyces. Mol Genet Genomics 265, 663-672.
35. Qu, X., Pang, B., Zhang, Z., Chen, M., Wu, Z., Zhao, Q., Zhang, Q., Wang, Y., Liu, Y. & Liu, W. (2012). Caerulomycins and collismycins share a common paradigm for 2,29-bipyridine biosynthesis via an unusual hybrid polyketide-peptide assembly logic. J Am Chem Soc 134, 9038-9041.
36. Quirós, L. M., Aguirrezabalaga, I., Olano, C., Méndez, C. & Salas, J. A. (1998). Two glycosyltransferases and a glycosidase are involved in oleandomycin modification during its biosynthesis by Streptomyces antibioticus. Mol Microbiol 28, 1177-1185.
37. Ramos, J. L., Martínez-Bueno, M., Molina-Henares, A. J., Terán, W., Watanabe, K., Zhang, X., Gallegos, M. T., Brennan, R. & Tobes, R. (2005). The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69, 326-356.
38. Rodríguez, M., Núñez, L. E., Braña, A. F., Méndez, C., Salas, J. A. & Blanco, G. (2008). Identification of transcriptional activators for thienamycin and cephamycin C biosynthetic genes within the thienamycin gene cluster from Streptomyces cattleya. Mol Microbiol 69, 633-645.
39. Salerno, P., Marineo, S. & Puglia, A. M. (2007). The Streptomyces coelicolor dnaK operon contains a second promoter driving the expression of the negative regulator hspR at physiological temperature. Arch Microbiol 188, 541-546.
40. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
41. Seipke, R. F., Song, L., Bicz, J., Laskaris, P., Yaxley, A. M., Challis, G. L. & Loria, R. (2011). The plant pathogen Streptomyces scabies 87-22 has a functional pyochelin biosynthetic pathway that is regulated by TetR-and AfsR-family proteins. Microbiology 157, 2681-2693.
42. Shindo, K., Yamagishi, Y., Okada, Y. & Kawai, H. (1994). Collismycins A and B, novel non-steroidal inhibitors of dexamethasone-glucocorticoid receptor binding. J Antibiot (Tokyo) 47, 1072-1074.
43. Sialer, C., García, I., González-Sabín, J., Braña, A. F., Méndez, C., Morís, F. & Salas, J. A. (2013). Generation by mutasynthesis of potential neuroprotectant derivatives of the bipyridyl collismycin A. Bioorg Med Chem Lett 23, 5707-5709.
44. Siebenberg, S., Bapat, P. M., Lantz, A. E., Gust, B. & Heide, L. (2010). Reducing the variability of antibiotic production in Streptomyces by cultivation in 24-square deepwell plates. J Biosci Bioeng 109, 230-234.
45. Stadler, M., Bauch, F., Henkel, T., Mühlbauer, A., Müller, H., Spaltmann, F. & Weber, K. (2001). Antifungal actinomycete metabolites discovered in a differential cell-based screening using a recombinant TOPO1 deletion mutant strain. Arch Pharm (Weinheim) 334, 143-147.
46. Stephens, D. L., Choe, M. D. & Earhart, C. F. (1995). Escherichia coli periplasmic protein FepB binds ferrienterobactin. Microbiology 141, 1647-1654.
47. Sun, Y., He, X., Liang, J., Zhou, X. & Deng, Z. (2009). Analysis of functions in plasmid pHZ1358 influencing its genetic and structural stability in Streptomyces lividans 1326. Appl Microbiol Biotechnol 82, 303-310.
48. Tsuge, N., Furihata, K., Shin-Ya, K., Hayakawa, Y. & Seto, H. (1999). Novel antibiotics pyrisulfoxin A and B produced by Streptomyces californicus. J Antibiot (Tokyo) 52, 505-507.
49. Vasanthakumar, A., Kattusamy, K. & Prasad, R. (2013). Regulation of daunorubicin biosynthesis in Streptomyces peucetius-feed forward and feedback transcriptional control. J Basic Microbiol 53, 636-644.
50. Yang, H., An, Y., Wang, L., Zhang, S., Zhang, Y., Tian, Y., Liu, G. & Tan, H. (2010). Autoregulation of hpdR and its effect on CDA biosynthesis in Streptomyces coelicolor. Microbiology 156, 2641-2648.
51. Zhu, Y., Fu, P., Lin, Q., Zhang, G., Zhang, H., Li, S., Ju, J., Zhu, W. & Zhang, C. (2012). Identification of caerulomycin A gene cluster implicates a tailoring amidohydrolase. Org Lett 14, 2666-2669.