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. 1997 Nov;179(22):6986–6993. doi: 10.1128/jb.179.22.6986-6993.1997

Butyrolactone autoregulator receptor protein (BarA) as a transcriptional regulator in Streptomyces virginiae.

H Kinoshita 1, H Ipposhi 1, S Okamoto 1, H Nakano 1, T Nihira 1, Y Yamada 1
PMCID: PMC179638  PMID: 9371444

Abstract

BarA of Streptomyces virginiae is a specific receptor protein for virginiae butanolides (VBs), a member of the butyrolactone autoregulators of Streptomyces species. Sequencing around the barA gene revealed two novel open reading frames: one upstream, barX, encoding a homolog of AfsA of Streptomyces griseus and another downstream, barB. Northern (RNA) blot analysis for S. virginiae demonstrated that the addition of VB during cultivation switched on the expression of barB. An in vivo expression system in Streptomyces lividans with the use of the xylE reporter gene indicated that BarA in conjunction with VB controlled the barB promoter. Furthermore, the DNA binding ability of BarA was demonstrated in vitro for the first time by means of surface plasmon resonance and a gel-shift assay. Complex formation with VB in vitro resulted in the dissociation of BarA from DNA, thus suggesting that the VB receptor, BarA, is a transcriptional regulator and that the VB signal is transduced to the next step in the signal transduction pathway by modification of the DNA binding ability of BarA.

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Selected References

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  1. Clayton T. M., Bibb M. J. Streptomyces promoter-probe plasmids that utilise the xylE gene of Pseudomonas putida. Nucleic Acids Res. 1990 Feb 25;18(4):1077–1077. doi: 10.1093/nar/18.4.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Garland P. B. Optical evanescent wave methods for the study of biomolecular interactions. Q Rev Biophys. 1996 Feb;29(1):91–117. doi: 10.1017/s0033583500005758. [DOI] [PubMed] [Google Scholar]
  3. Gräfe U., Schade W., Eritt I., Fleck W. F., Radics L. A new inducer of anthracycline biosynthesis from Streptomyces viridochromogenes. J Antibiot (Tokyo) 1982 Dec;35(12):1722–1723. doi: 10.7164/antibiotics.35.1722. [DOI] [PubMed] [Google Scholar]
  4. Guilfoile P. G., Hutchinson C. R. Sequence and transcriptional analysis of the Streptomyces glaucescens tcmAR tetracenomycin C resistance and repressor gene loci. J Bacteriol. 1992 Jun;174(11):3651–3658. doi: 10.1128/jb.174.11.3651-3658.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Guilfoile P. G., Hutchinson C. R. The Streptomyces glaucescens TcmR protein represses transcription of the divergently oriented tcmR and tcmA genes by binding to an intergenic operator region. J Bacteriol. 1992 Jun;174(11):3659–3666. doi: 10.1128/jb.174.11.3659-3666.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hillen W., Berens C. Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Annu Rev Microbiol. 1994;48:345–369. doi: 10.1146/annurev.mi.48.100194.002021. [DOI] [PubMed] [Google Scholar]
  7. Hinrichs W., Kisker C., Düvel M., Müller A., Tovar K., Hillen W., Saenger W. Structure of the Tet repressor-tetracycline complex and regulation of antibiotic resistance. Science. 1994 Apr 15;264(5157):418–420. doi: 10.1126/science.8153629. [DOI] [PubMed] [Google Scholar]
  8. Horinouchi S., Beppu T. Autoregulatory factors and communication in actinomycetes. Annu Rev Microbiol. 1992;46:377–398. doi: 10.1146/annurev.mi.46.100192.002113. [DOI] [PubMed] [Google Scholar]
  9. Horinouchi S., Suzuki H., Nishiyama M., Beppu T. Nucleotide sequence and transcriptional analysis of the Streptomyces griseus gene (afsA) responsible for A-factor biosynthesis. J Bacteriol. 1989 Feb;171(2):1206–1210. doi: 10.1128/jb.171.2.1206-1210.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ingram C., Brawner M., Youngman P., Westpheling J. xylE functions as an efficient reporter gene in Streptomyces spp.: use for the study of galP1, a catabolite-controlled promoter. J Bacteriol. 1989 Dec;171(12):6617–6624. doi: 10.1128/jb.171.12.6617-6624.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kim H. S., Nihira T., Tada H., Yanagimoto M., Yamada Y. Identification of binding protein of virginiae butanolide C, an autoregulator in virginiamycin production, from Streptomyces virginiae. J Antibiot (Tokyo) 1989 May;42(5):769–778. doi: 10.7164/antibiotics.42.769. [DOI] [PubMed] [Google Scholar]
  12. Kim H. S., Tada H., Nihira T., Yamada Y. Purification and characterization of virginiae butanolide C-binding protein, a possible pleiotropic signal-transducer in Streptomyces virginiae. J Antibiot (Tokyo) 1990 Jun;43(6):692–706. doi: 10.7164/antibiotics.43.692. [DOI] [PubMed] [Google Scholar]
  13. Kisker C., Hinrichs W., Tovar K., Hillen W., Saenger W. The complex formed between Tet repressor and tetracycline-Mg2+ reveals mechanism of antibiotic resistance. J Mol Biol. 1995 Mar 24;247(2):260–280. doi: 10.1006/jmbi.1994.0138. [DOI] [PubMed] [Google Scholar]
  14. Kondo K., Higuchi Y., Sakuda S., Nihira T., Yamada Y. New virginiae butanolides from Streptomyces virginiae. J Antibiot (Tokyo) 1989 Dec;42(12):1873–1876. doi: 10.7164/antibiotics.42.1873. [DOI] [PubMed] [Google Scholar]
  15. Miyake K., Horinouchi S., Yoshida M., Chiba N., Mori K., Nogawa N., Morikawa N., Beppu T. Detection and properties of A-factor-binding protein from Streptomyces griseus. J Bacteriol. 1989 Aug;171(8):4298–4302. doi: 10.1128/jb.171.8.4298-4302.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nihira T., Shimizu Y., Kim H. S., Yamada Y. Structure-activity relationships of virginiae butanolide C, an inducer of virginiamycin production in Streptomyces virginiae. J Antibiot (Tokyo) 1988 Dec;41(12):1828–1837. doi: 10.7164/antibiotics.41.1828. [DOI] [PubMed] [Google Scholar]
  17. Okamoto S., Nakamura K., Nihira T., Yamada Y. Virginiae butanolide binding protein from Streptomyces virginiae. Evidence that VbrA is not the virginiae butanolide binding protein and reidentification of the true binding protein. J Biol Chem. 1995 May 19;270(20):12319–12326. doi: 10.1074/jbc.270.20.12319. [DOI] [PubMed] [Google Scholar]
  18. Okamoto S., Nihira T., Kataoka H., Suzuki A., Yamada Y. Purification and molecular cloning of a butyrolactone autoregulator receptor from Streptomyces virginiae. J Biol Chem. 1992 Jan 15;267(2):1093–1098. [PubMed] [Google Scholar]
  19. Onaka H., Ando N., Nihira T., Yamada Y., Beppu T., Horinouchi S. Cloning and characterization of the A-factor receptor gene from Streptomyces griseus. J Bacteriol. 1995 Nov;177(21):6083–6092. doi: 10.1128/jb.177.21.6083-6092.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pan W., Spratt B. G. Regulation of the permeability of the gonococcal cell envelope by the mtr system. Mol Microbiol. 1994 Feb;11(4):769–775. doi: 10.1111/j.1365-2958.1994.tb00354.x. [DOI] [PubMed] [Google Scholar]
  21. Rao R. N., Richardson M. A., Kuhstoss S. Cosmid shuttle vectors for cloning and analysis of Streptomyces DNA. Methods Enzymol. 1987;153:166–198. doi: 10.1016/0076-6879(87)53053-1. [DOI] [PubMed] [Google Scholar]
  22. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  23. Unger B., Becker J., Hillen W. Nucleotide sequence of the gene, protein purification and characterization of the pSC101-encoded tetracycline resistance-gene-repressor. Gene. 1984 Nov;31(1-3):103–108. doi: 10.1016/0378-1119(84)90199-9. [DOI] [PubMed] [Google Scholar]
  24. Waki M., Nihira T., Yamada Y. Cloning and characterization of the gene (farA) encoding the receptor for an extracellular regulatory factor (IM-2) from Streptomyces sp. strain FRI-5. J Bacteriol. 1997 Aug;179(16):5131–5137. doi: 10.1128/jb.179.16.5131-5137.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yamada Y., Sugamura K., Kondo K., Yanagimoto M., Okada H. The structure of inducing factors for virginiamycin production in Streptomyces virginiae. J Antibiot (Tokyo) 1987 Apr;40(4):496–504. doi: 10.7164/antibiotics.40.496. [DOI] [PubMed] [Google Scholar]
  26. Yang K., Han L., Vining L. C. Regulation of jadomycin B production in Streptomyces venezuelae ISP5230: involvement of a repressor gene, jadR2. J Bacteriol. 1995 Nov;177(21):6111–6117. doi: 10.1128/jb.177.21.6111-6117.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]

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