Structure of the branched-chain Amino Acid and GTP-sensing global regulator, cody, from bacillus subtilis

Journal of Biological Chemistry

Volumn 292, Issue 7, 2017, Pages 2714-2728

  Levdikov, Vladimir M ^a   Blagova, Elena ^a   Young, Vicki L ^b   Belitsky, Boris R ^c   Lebedev, Andrey ^b   Sonenshein, Abraham L ^a   Wilkinson, Anthony J ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RUTHERFORD APPLETON LABORATORY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIOLOGY; ELECTROPHORETIC MOBILITY; LIGHT SCATTERING; ORGANIC POLYMERS; SIZE EXCLUSION CHROMATOGRAPHY; TRANSCRIPTION;

BRANCHED CHAIN AMINO ACIDS; ELECTROPHORETIC MOBILITY SHIFT; GLOBAL REGULATORS; GRAM-POSITIVE BACTERIUM; MULTIANGLE LASER LIGHT SCATTERING; NUTRIENT LIMITATIONS; PHOSPHODIESTERASES; TRANSCRIPTIONAL CHANGES;

CRYSTAL STRUCTURE;

ADENYLATE CYCLASE; BRANCHED CHAIN AMINO ACID; GUANOSINE TRIPHOSPHATE; PROTEIN CODY; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; LIGAND; PROTEIN BINDING;

ALPHA HELIX; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL STRAIN; BINDING AFFINITY; CELL LEVEL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CRYSTALLIZATION; LIGHT SCATTERING; MULTIANGLE LASER LIGHT SCATTERING; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIZE EXCLUSION CHROMATOGRAPHY; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

AMINO ACIDS, BRANCHED-CHAIN; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; LIGANDS; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 85013468465     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.754309     Document Type: Article

References (61)

1. Slack, F., Serror, P., Joyce, E., and Sonenshein, A. L. (1995) A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol. Microbiol. 15, 689-702
2. Molle, V., Nakaura, Y., Shivers, R. P., Yamaguchi, H., Losick, R., Fujita, Y., and Sonenshein, A. L. (2003) Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J. Bacteriol. 185, 1911-1922
3. Brinsmade, S. R., Alexander, E. L., Livny, J., Stettner, A. I., Segrè, D., Rhee, K. Y., and Sonenshein, A. L. (2014) Hierarchical expression of genes controlled by the Bacillus subtilis global regulatory protein CodY. Proc. Natl. Acad. Sci. U.S.A. 111, 8227-8232
4. Pohl, K., Francois, P., Stenz, L., Schlink, F., Geiger, T., Herbert, S., Goerke, C., Schrenzel, J., and Wolz, C. (2009) CodY in Staphylococcus aureus: a regulatory link between metabolism and virulence gene expression. J. Bacteriol. 191, 2953-2963
5. Majerczyk, C. D., Sadykov, M. R., Luong, T. T., Lee, C., Somerville, G. A., and Sonenshein, A. L. (2008) Staphylococcus aureus CodY negatively regulates virulence gene expression. J. Bacteriol. 190, 2257-2265
6. Hendriksen, W. T., Bootsma, H. J., Estevão, S., Hoogenboezem, T., de Jong, A., de Groot, R., Kuipers, O. P., and Hermans, P. W. (2008) CodY of Streptococcus pneumoniae: link between nutritional gene regulation and colonization. J. Bacteriol. 190, 590- 601
7. Malke, H., Steiner, K., McShan, W. M., and Ferretti, J. J. (2006) Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: the action of CodY and RelA. Int. J. Med. Microbiol. 296, 259-275
8. Lobel, L., Sigal, N., Borovok, I., Ruppin, E., and Herskovits, A. A. (2012) Integrative genomic analysis identifies isoleucine and CodY as regulators of Listeria monocytogenes virulence. PLoS Genet. 8, e1002887
9. Bennett, H. J., Pearce, D. M., Glenn, S., Taylor, C. M., Kuhn, M., Sonenshein, A. L., Andrew, P. W., and Roberts, I. S. (2007) Characterisation of relA and codY mutants of Listeria monocytogenes: identification of the CodY regulon and its role in virulence. Mol. Microbiol. 63, 1453-1467
10. van Schaik, W., Château, A., Dillies, M. A., Coppée, J. Y., Sonenshein, A. L., and Fouet, A. (2009) The global regulator CodY regulates toxin gene expression in Bacillus anthracis and is required for full virulence. Infect. Immun. 77, 4437- 4445
11. Dineen, S. S., McBride, S. M., and Sonenshein, A. L. (2010) Integration of metabolism and virulence by Clostridium difficile CodY. J. Bacteriol. 192, 5350-5362
12. Sonenshein, A. L. (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr. Opin. Microbiol. 8, 203-207
13. Shivers, R. P., and Sonenshein, A. L. (2004) Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol. Microbiol. 53, 599-611
14. Ratnayake-Lecamwasam, M., Serror, P., Wong, K. W., and Sonenshein, A. L. (2001) Bacillus subtilis CodY represses early stationary-phase genes by sensing GTP levels. Genes Dev. 15, 1093-1103
15. Belitsky, B. R., and Sonenshein, A. L. (2011) Roadblock repression of transcription by Bacillus subtilis CodY. J. Mol. Biol. 411, 729-743
16. Shivers, R. P., Dineen, S. S., and Sonenshein, A. L. (2006) Positive regulation of Bacillus subtilis ackA by CodY and CcpA: establishing a potential hierarchy in carbon flow. Mol. Microbiol. 62, 811-822
17. Preis, H., Eckart, R. A., Gudipati, R. K., Heidrich, N., and Brantl, S. (2009) CodY activates transcription of a small RNA in Bacillus subtilis. J. Bacteriol. 191, 5446-5457
18. den Hengst, C. D., van Hijum, S. A., Geurts, J. M., Nauta, A., Kok, J., and Kuipers, O. P. (2005) The Lactococcus lactis CodY regulon: identification of a conserved cis-regulatory element. J. Biol. Chem. 280, 34332-34342
19. Guédon, E., Sperandio, B., Pons, N., Ehrlich, S. D., and Renault, P. (2005) Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151, 3895-3909
20. Belitsky, B. R., and Sonenshein, A. L. (2008) Genetic and biochemical analysis of CodY-binding sites in Bacillus subtilis. J. Bacteriol. 190, 1224-1236
21. Nicolas, P., Mäder, U., Dervyn, E., Rochat, T., Leduc, A., Pigeonneau, N., Bidnenko, E., Marchadier, E., Hoebeke, M., Aymerich, S., Becher, D., Bisicchia, P., Botella, E., Delumeau, O., Doherty, G., et al. (2012) Conditiondependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335, 1103-1106
22. Belitsky, B. R., and Sonenshein, A. L. (2013) Genome-wide identification of Bacillus subtilis CodY-binding sites at single-nucleotide resolution. Proc. Natl. Acad. Sci. U.S.A. 110, 7026-7031
23. Levdikov, V. M., Blagova, E., Joseph, P., Sonenshein, A. L., and Wilkinson, A. J. (2006) The structure of CodY, a GTP- and isoleucine-responsive regulator of stationary phase and virulence in Gram-positive bacteria. J. Biol. Chem. 281, 11366-11373
24. Aravind, L., and Ponting, C. P. (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem. Sci. 22, 458-459
25. Levdikov, V. M., Blagova, E., Colledge, V. L., Lebedev, A. A., Williamson, D. C., Sonenshein, A. L., and Wilkinson, A. J. (2009) Structural rearrangement accompanying ligand binding in the GAF domain of CodY from Bacillus subtilis. J. Mol. Biol. 390, 1007-1018
26. Blagova, E. V., Levdikov, V. M., Tachikawa, K., Sonenshein, A. L., and Wilkinson, A. J. (2003) Crystallization of the GTP-dependent transcriptional regulator CodY from Bacillus subtilis. Acta Crystallogr. D Biol. Crystallogr. 59, 155-157
27. Villapakkam, A. C., Handke, L. D., Belitsky, B. R., Levdikov, V. M., Wilkinson, A. J., and Sonenshein, A. L. (2009) Genetic and biochemical analysis of the interaction of Bacillus subtilis CodY with branched-chain amino acids. J. Bacteriol. 191, 6865- 6876
28. Belitsky, B. R., Brinsmade, S. R., and Sonenshein, A. L. (2015) Intermediate levels of Bacillus subtilis CodY activity are required for derepression of the branched-chain amino acid permease, BraB. PLoS Genet. 11, e1005600
29. Belitsky, B. R. (2015) Role of branched-chain amino acid transport in Bacillus subtilis CodY activity. J. Bacteriol. 197, 1330-1338
30. Maass, S., Wachlin, G., Bernhardt, J., Eymann, C., Fromion, V., Riedel, K., Becher, D., and Hecker, M. (2014) Highly precise quantification of protein molecules per cell during stress and starvation responses in Bacillus subtilis. Mol. Cell. Proteomics 13, 2260-2276
31. Belitsky, B. R., and Sonenshein, A. L. (2011) Contributions of multiple binding sites and effector-independent binding to CodY-mediated regulation in Bacillus subtilis. J. Bacteriol. 193, 473-484
32. Lewis, R. J., Muchová, K., Brannigan, J. A., Barák, I., Leonard, G., and Wilkinson, A. J. (2000) Domain swapping in the sporulation response regulator Spo0A. J. Mol. Biol. 297, 757-770
33. Levdikov, V. M., Blagova, E. V., Rawlings, A. E., Jameson, K., Tunaley, J., Hart, D. J., Barak, I., and Wilkinson, A. J. (2012) Structure of the phosphatase domain of the cell fate determinant SpoIIE from Bacillus subtilis. J. Mol. Biol. 415, 343-358
34. Travers, A. A., and Klug, A. (1987) The bending of DNA in nucleosomes and its wider implications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 317, 537-561
35. Ji, Q., Zhang, L., Jones, M. B., Sun, F., Deng, X., Liang, H., Cho, H., Brugarolas, P., Gao, Y. N., Peterson, S. N., Lan, L., Bae, T., and He, C. (2013) Molecular mechanism of quinone signaling mediated through S-quinonization of a YodB family repressor QsrR. Proc. Natl. Acad. Sci. U.S.A. 110, 5010-5015
36. van Aalten, D. M., DiRusso, C. C., and Knudsen, J. (2001) The structural basis of acyl coenzyme A-dependent regulation of the transcription factor FadR. EMBO J. 20, 2041-2050
37. Rajagopalan, S., Teter, S. J., Zwart, P. H., Brennan, R. G., Phillips, K. J., and Kiley, P. J. (2013) Studies of IscR reveal a unique mechanism for metal-dependent regulation of DNA binding specificity. Nat. Struct. Mol. Biol. 20, 740-747
38. Santos, J. A., Alonso-García, N., Macedo-Ribeiro, S., and Pereira, P. J. (2014) The unique regulation of iron-sulfur cluster biogenesis in a Grampositive bacterium. Proc. Natl. Acad. Sci. U.S.A. 111, E2251-E2260
39. Wray, L. V., Jr., and Fisher, S. H. (2011) Bacillus subtilis CodY operators contain overlapping CodY binding sites. J. Bacteriol. 193, 4841- 4848
40. Babu, Y. S., Bugg, C. E., and Cook, W. J. (1988) Structure of calmodulin refined at 2.2 A resolution. J. Mol. Biol. 204, 191-204
41. Drum, C. L., Yan, S. Z., Bard, J., Shen, Y. Q., Lu, D., Soelaiman, S., Grabarek, Z., Bohm, A., and Tang, W. J. (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415, 396-402
42. Wilkinson, A. J. (1996) Accommodating structurally diverse peptides in proteins. Chem. Biol. 3, 519-524
43. Han, A. R., Kang, H. R., Son, J., Kwon, D. H., Kim, S., Lee, W. C., Song, H. K., Song, M. J., and Hwang, K. Y. (2016) The structure of the pleiotropic transcription regulator CodY provides insight into its GTP-sensing mechanism. Nucleic Acids Res. 44, 9483-9493
44. Zeigler, D. R., Prágai, Z., Rodriguez, S., Chevreux, B., Muffler, A., Albert, T., Bai, R., Wyss, M., and Perkins, J. B. (2008) The origins of 168, W23, and other Bacillus subtilis legacy strains. J. Bacteriol. 190, 6983- 6995
45. Atkinson, M. R., Wray, L. V., Jr, and Fisher, S. H. (1990) Regulation of histidine and proline degradation enzymes by amino acid availability in Bacillus subtilis. J. Bacteriol. 172, 4758-4765
46. Fouet, A., and Sonenshein, A. L. (1990) A target for carbon source-dependent negative regulation of the citB promoter of Bacillus subtilis. J. Bacteriol. 172, 835-844
47. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119
48. Miller, J. H. (1972) Experiments in Molecular Genetics, p. 433, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
49. Sambrook, J., Fritsch, E. F., and Maniatis, T. J. (1989) Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
50. Guzman, L. M., Belin, D., Carson, M. J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121- 4130
51. Fogg, M. J., and Wilkinson, A. J. (2008) Higher-throughput approaches to crystallization and crystal structure determination. Biochem. Soc. Trans. 36, 771-775
52. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol. 276, 307-326
53. Lebedev, A. A., and Isupov, M. N. (2014) Space-group and origin ambiguity in macromolecular structures with pseudo-symmetry and its treatment with the program Zanuda. Acta Crystallogr. D Biol. Crystallogr. 70, 2430-2443
54. Vagin, A., and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25
55. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
56. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
57. McNicholas, S., Potterton, E., Wilson, K. S., and Noble, M. E. (2011) Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr. D Biol. Crystallogr. 67, 386-394
58. Wen, J., and Arakawa, T. (2000) Refractive index of proteins in aqueous sodium chloride. Anal. Biochem. 280, 327-329
59. Nicolai, T., van Dijk, T. N., van Dijk, J. A., and Smit, J. A. (1987) Molar mass characterization of DNA fragments by gel permeation chromatography using a low-angle laser light-scattering detector. J. Chromatogr. 389, 286-292
60. Belitsky, B. R. (2011) Indirect repression by Bacillus subtilis CodY via displacement of the activator of the proline utilization operon. J. Mol. Biol. 413, 321-336
61. Belitsky, B. R., and Sonenshein, A. L. (1998) Role and regulation of Bacillus subtilis glutamate dehydrogenase genes. J. Bacteriol. 180, 6298-6305