Structural and functional basis of transcriptional regulation by TetR family protein CprB from S. coelicolorA3(2)

Nucleic Acids Research

Volumn 42, Issue 15, 2014, Pages 10122-10133

  Bhukya, Hussain ^a,b   Bhujbalrao, Ruchika ^a   Bitra, Aruna ^a   Anand, Ruchi ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

^b IITB MONASH RESEARCH ACADEMY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CPRB PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; APOPROTEIN; BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA PROTEIN COMPLEX; DNA SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; STREPTOMYCES COELICOLOR; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; CHEMICAL STRUCTURE; CHEMISTRY; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

APOPROTEINS; BACTERIAL PROTEINS; BASE SEQUENCE; CONSENSUS SEQUENCE; DNA, BACTERIAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MUTAGENESIS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84920894689     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku587     Document Type: Article

References (71)

1. Berdy, J. (2005) Bioactive microbial metabolites. J. Antibiot., 58, 1-26.
2. Walsh, C.T. (2003) Antibiotics: Actions, Origins, Resistance. ASM Press, Washington, DC, USA.
3. Bassler, B.L. and Losick, R. (2006) Bacterially speaking. Cell, 125, 237-246.
4. Camilli, A. and Bassler, B.L. (2006) Bacterial small-molecule signaling pathways. Science, 311, 1113-1116.
5. Willey, J.M. and Gaskell, A.A. (2011) Morphogenetic signaling molecules of the Streptomycetes. Chem. Rev., 111, 174-187.
6. Horinouchi, S. (2002) A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus. Front. Biosci, 7, 2045-2057.
7. Onaka, H., Ando, N., Nihira, T., Yamada, Y, Beppu, T. and Horinouchi, S. (1995) Cloning and characterization of the A-factor receptor gene from Streptomyces griseus. J. Bacteriol., 177, 6083-6092.
8. Khokhlov, A.S., Tovarova, I., Borisova, L.N., Pliner, S.A., Shevchenko, L.N., Kornitskaia, E., Ivkina, N.S. and Rapoport, I.A. (1967) The A-factor, responsible for streptomycin biosynthesis by mutant strains of Actinomyces streptomycini. Dokl. Akad. Nauk. SSSR, 177, 232-235.
9. Khokhlov, A.S., Anisova, L.N., Tovarova, I.I., Kleiner, E.M., Kovalenko, I.V., Krasilnikova, O.I., Kornitskaya, E.Y and Pliner, S.A. (1973) Effect of A-factor on the growth of asporogenous mutants of Streptomyces griseus, not producing this factor. Z. Allg. Mikrobiol., 13, 647-655.
10. Ohnishi, Y, Yamazaki, H., Kato, J.-Y, Tomono, A. and Horinouchi, S. (2005) AdpA, a central transcriptional regulator in the A-factor regulatory cascade that leads to morphological development and secondary metabolism in Streptomyces griseus. Biosci. Biotech. Biochem., 69, 431-439.
11. Onaka, H. and Horinouchi, S. (1997) DNA-binding activity of the A-factor receptor protein and its recognition DNA sequences. Mol Microbiol, 24, 991-1000.
12. Ohnishi, Y, Kameyama, S., Onaka, H. and Horinouchi, S. (1999) The A-factor regulatory cascade leading to streptomycin biosynthesis in Streptomyces griseus: identification of a target gene of the A-factor receptor. Mol Microbiol, 34, 102-111.
13. Kitani, S., Kinoshita, H., Nihira, T and Yamada, Y (1999) In vitro analysis of the butyrolactone autoregulator receptor protein (FarA) of Streptomyces lavendulae FRI-5 reveals that FarA acts as a DNA-Binding transcriptional regulator that controls its own synthesis. J. Bacteriol, 181, 5081-5084.
14. Kinoshita, H., Ipposhi, H., Okamoto, S., Nakano, H., Nihira, T and Yamada, Y (1997) Butyrolactone autoregulator receptor protein (BarA) as a transcriptional regulator in Streptomyces virginiae. J. Bacteriol, 179, 6986-6993.
15. Nakano, H., Takehara, E., Nihira, T and Yamada, Y (1998) Gene replacement analysis of the Streptomyces virginiae barA Gene encoding the butyrolactone autoregulator receptor reveals that BarA acts as a repressor in virginiamycin biosynthesis. J. Bacteriol, 180, 3317-3322.
16. Stratigopoulos, G, Gandecha, A.R. and Cundliffe, E. (2002) Regulation of tylosin production and morphological differentiation in Streptomyces fradiae by TylP, a deduced γ-butyrolactone receptor. Mol Microbiol, 45, 735-744.
17. Williamson, N.R., Fineran, PC, Leeper, F.J. and Salmond, GPC (2006) The biosynthesis and regulation of bacterial prodiginines. Nat. Rev. Microbiol, 4, 887-899.
18. Xu, G, Wang, J., Wang, L., Tian, X., Yang, H., Fan, K., Yang, K. and Tan, H. (2010) 'Pseudo' γ - butyrolactone receptors respond to antibiotic signals to coordinate antibiotic biosynthesis. J. Biol. Chem., 285, 27 440-27 448.
19. Onaka, H., Nakagawa, T and Horinouchi, S. (1998) Involvement of two A-factor receptor homologues in Streptomyces coelicolor A3(2) in the regulation of secondary metabolism and morphogenesis. Mol Microbiol, 28, 743-753.
20. Takano, E., Chakraburtty, R., Nihira, T, Yamada, Y and Bibb, M.J. (2001) A complex role for the γ - butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol, 41, 1015-1028.
21. Natsume, R., Ohnishi, Y, Senda, T and Horinouchi, S. (2004) Crystal structure of a γ - butyrolactone autoregulator receptor protein in Streptomyces coelicolor A3(2). J. Mol Biol, 336, 409-419.
22. Takano, E. (2006) γ - Butyrolactones: Streptomyces signalling molecules regulating antibiotic production and differentiation. Curr Opin. Microbiol, 9, 287-294.
23. Takano, E., Kinoshita, H., Mersinias, V, Bucca, G, Hotchkiss, G, Nihira, T, Smith, CP, Bibb, M., Wohlleben, W. and Chater, K. (2005) A bacterial hormone (the SCB1) directly controls the expression of a pathway-specific regulatory gene in the cryptic type I polyketide biosynthetic gene cluster of Streptomyces coelicolor. Mol Microbiol., 56, 465-479.
24. Wang, J., Wang, W., Wang, L., Zhang, G, Fan, K., Tan, H. and Yang, K. (2011) A novel role of'pseudo' γ - butyrolactone receptors in controlling γ - butyrolactone biosynthesis in Streptomyces. Mol Microbiol, 82, 236-250.
25. Ramos, J.L., Martinez-Bueno, M., Molina-Henares, A.J., Teran, W., Watanabe, K., Zhang, X., Gallegos, M.T, Brennan, R. and Tobes, R. (2005) The TetR family of transcriptional repressors. Microbiol. Mol Biol. Rev, 69, 326-356.
26. Cuthbertson, L. and Nodwell, J.R. (2013) The TetR family of regulators. Microbiol. Mol Biol. Rev, 77, 440-475.
27. Orth, P, Schnappinger, D., Hillen, W., Saenger, W. and Hinrichs, W (2000) Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat. Struct. Mol Biol, 7, 215-219.
28. Schumacher, M.A., Miller, M.C, Grkovic, S., Brown, M.H., Skurray, R.A. and Brennan, R.G (2002) Structural basis for cooperative DNA binding by two dimers of the multidrug-binding protein QacR. EMBO J., 21, 1210-1218.
29. Miller, DJ, Zhang, Y-M., Subramanian, C, Rock, CO. and White, S.W. (2010) Structural basis for the transcriptional regulation of membrane lipid homeostasis. Nat. Struct. Mol Biol, 17, 971-975.
30. Itou, H., Watanabe, N, Yao, M., Shirakihara, Y and Tanaka, I. (2010) Crystal structures of the multidrug binding repressor Corynebacterium glutamicum CgmR in complex with inducers and with an operator. J. Mol Biol, 403, 174-184.
31. Le, TB.K., Schumacher, M.A., Lawson, D.M., Brennan, R.G and Buttner, M.J. (2011) The crystal structure of the TetR family transcriptional repressor SimR bound to DNA and the role of a flexible N-terminal extension in minor groove binding. Nucleic Acids Res., 39, 9433-9447.
32. Tonthat, NK, Milam, S.L., Chinnam, N, Whitfill, T, Margolin, W. and Schumacher, M.A. (2013) SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proc. Natl Acad. Sci. U.S.A., 110, 10 586-10 591.
33. Yang, S., Gao, Z., Li, T, Yang, M., Zhang, T, Dong, Y and He, ZG (2013) Structural basis for interaction between Mycobacterium smegmatis Ms6564, a TetR family master regulator, and its target DNA. J. Biol. Chem., 288, 23 687-23 695.
34. McMurry, L., Petrucci, R.E. and Levy, S.B. (1980) Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc. Natl Acad. Sci. U.S.A., 77, 3974-3977.
35. Yamaguchi, A., Iwasaki-Ohba, Y, Ono, N, Kaneko-Ohdera, M. and Sawai, T (1991) Stoichiometry of metal-tetracycline/H +antiport mediated by transposon Tn10-encoded tetracycline resistance protein in Escherichia coli. FEBSLett., 282, 415-418.
36. Bertrand, K.P., Postle, K., Wray, L.V Jr and Reznikoff, W.S. (1983) Overlapping divergent promoters control expression of Tn10 tetracycline resistance. Gene, 23, 149-156.
37. Hinrichs, W., Kisker, C, Duvel, M., Muller, A., Tovar, K., Hillen, W. and Saenger, W. (1994) Structure of the Tet repressor-tetracycline complex and regulation of antibiotic resistance. Science, 264, 418-420.
38. 2+ reveals mechanism of antibiotic resistance. J. Mol. Biol., 247, 260-280.
39. Le, T.B.K., Stevenson, C.E.M., Fiedler, H.-P., Maxwell, A., Lawson, D.M. and Buttner, M.J. (2011) Structures of the TetR-like simocyclinone efflux pump repressor, SimR, and the mechanism of ligand-mediated derepression. J. Mol. Biol., 408, 40-56.
40. Schumacher, M.A., Miller, M.C., Grkovic, S., Brown, M.H., Skurray, R.A. and Brennan, R.G. (2001) Structural mechanisms of QacR induction and multidrug recognition. Science, 294, 2158-2163.
41. Zhang, Y.-M., Zhu, K., Frank, M.W. and Rock, C.O. (2007) A Pseudomonas aeruginosa transcription factor that senses fatty acid structure. Mol. Microbiol., 66, 622-632.
42. Cho, H., McManus, H.R., Dove, S.L. and Bernhardt, T.G. (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc. Natl Acad. Sci. U.S.A., 108, 3773-3778.
43. Tonthat, N.K., Arold, S.T., Pickering, B.F., Van Dyke, M.W., Liang, S., Lu, Y., Beuria, T.K., Margolin, W. and Schumacher, M.A. (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J., 30, 154-164.
44. Yang, M., Gao, C., Cui, T., An, J. and He, Z.-G. (2012) A TetR-like regulator broadly affects the expressions of diverse genes in Mycobacterium smegmatis. Nucleic Acids Res., 40, 1009-1020.
45. Natsume, R., Takeshita, R., Sugiyama, M., Ohnishi, Y., Senda, T. and Horinouchi, S. (2003) Crystallization of CprB, an autoregulator-receptor protein from Streptomyces coelicolor A3(2). Acta Crystallogr. D Biol. Crystallogr., 59, 2313-2315.
46. Sugiyama, M., Onaka, H., Nakagawa, T. and Horinouchi, S. (1998) Site-directed mutagenesis of the A-factor receptor protein: Val-41 important for DNA-binding and Trp-119 important for ligand-binding. Gene, 222, 133-144.
47. Battye, T.G.G., Kontogiannis, L., Johnson, O., Powell, H.R. and Leslie, A.G.W. (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr., 67, 271-281.
48. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr., 62, 72-82.
49. Panjikar, S., Parthasarathy, V., Lamzin, V.S., Weiss, M.S. and Tucker, P.A. (2005) Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr. D Biol. Crystallogr., 61, 449-457.
50. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr., 66, 486-501.
51. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
52. Murshudov, G.N., Skubak, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F. and Vagin, A.A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr., 67, 355-367.
53. Delano, W.L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.
54. Zheng, G., Lu, X.-J. and Olson, W.K. (2009) Web 3DNA-a web server for the analysis, reconstruction, and visualization of three-dimensional nucleic-acid structures. Nucleic Acids Res., 37, W240-W246.
55. Schmidt, B., Ho, L. and Hogg, P.J. (2006) Allosteric disulfide bonds. Biochemistry, 45, 7429-7433.
56. Wouters, M.A., Fan, S.W. and Haworth, N.L. (2010) Disulfides as redox switches: from molecular mechanisms to functional significance. Antioxid. Redox Signal., 12, 53-91.
57. Agari, Y., Sakamoto, K., Yutani, K., Kuramitsu, S. and Shinkai, A. (2013) Structure and function of a TetR family transcriptional regulator, SbtR, from Thermus thermophilus HB8. Proteins, 81, 1166-1178.
58. Yang, Y.H., Joo, H.S., Lee, K., Liou, K.K., Lee, H.C., Sohng, J.K. and Kim, B.-G. (2005) Novel method for detection of butanolides in Streptomyces coelicolor culture broth, using a His-tagged receptor (ScbR) and mass spectrometry. Appl. Environ. Microbiol., 71, 5050-5055.
59. Grkovic, S., Brown, M.H., Schumacher, M.A., Brennan, R.G. and Skurray, R.A. (2001) The Staphylococcal QacR multidrug regulator binds a correctly spaced operator as a pair of dimers. J. Bacteriol., 183, 7102-7109.
60. Reichheld, S.E., Yu, Z. and Davidson, A.R. (2009) The induction of folding cooperativity by ligand binding drives the allosteric response of tetracycline repressor. Proc. Natl Acad. Sci. U.S.A., 106, 22 263-22 268.
61. Daber, R., Stayrook, S., Rosenberg, A. and Lewis, M. (2007) Structural analysis of Lac repressor bound to allosteric effectors. J. Mol. Biol., 370, 609-619.
62. Lu, D., Fillet, S., Meng, C., Alguel, Y., Kloppsteck, P., Bergeron, J., Krell, T., Gallegos, M.T., Ramos, J. and Zhang, X. (2010) Crystal structure of TtgV in complex with its DNA operator reveals a general model for cooperative DNA binding of tetrameric gene regulators. Genes Dev., 24, 2556-2565.
63. Tahlan, K., Yu, Z., Xu, Y., Davidson, A.R. and Nodwell, J.R. (2008) Ligand recognition by ActR, a TetR-like regulator of actinorhodin export. J. Mol. Biol., 383, 753-761.
64. Xu, D., Seghezzi, N., Esnault, C. and Virolle, M.-J. (2010) Repression of antibiotic production and sporulation in Streptomyces coelicolor by overexpression of a TetR family transcriptional regulator. Appl. Environ. Microbiol., 76, 7741-7753.
65. Sola-Landa, A., Rodríguez-García, A., Franco-Domínguez, E. and Martín, J.F. (2005) Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol. Microbiol., 56, 1373-1385.
66. Salerno, P., Marineo, S. and Puglia, A. (2007) The Streptomyces coelicolor dnaK operon contains a second promoter driving the expression of the negative regulator hspR at physiological temperature. Archiv. Microbiol., 188, 541-546.
67. Bignell, D.R.D., Bate, N. and Cundliffe, E. (2007) Regulation of tylosin production: role of a TylP-interactive ligand. Mol. Microbiol., 63, 838-847.
68. Santamarta, I., Rodriguez-Garcia, A., Perez-Redondo, R., Martin, J.F. and Liras, P. (2002) CcaR is an autoregulatory protein that binds to the ccaR and cefD-cmcI promoters of the cephamycin C-clavulanic acid cluster in Streptomyces clavuligerus. J. Bacteriol., 184, 3106-3113.
69. Meier, I., Wray, L.V. and Hillen, W. (1988) Differential regulation of the Tn 10-encoded tetracycline resistance genes tetA and tetR by the tandem tet operators O1 and O2. EMBO J., 7, 567-572.
70. Kojic, M., Aguilar, C. and Venturi, V. (2002) TetR family member PsrA directly binds the Pseudomonas rpoS and psrA promoters. J. Bacteriol., 184, 2324-2330.
71. Liu, G., Chater, K.F., Chandra, G., Niu, G. and Tan, H. (2013) Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol. Mol. Biol. Rev., 77, 112-143.