Bacillus subtilis PhoP binds to the phoB tandem promoter exclusively within the phosphate starvation-inducible promoter

Journal of Bacteriology

Volumn 179, Issue 20, 1997, Pages 6302-6310

  Liu, Wei ^a   Hulett, F Marrion ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACILLUS SUBTILIS; BACTERIUM CULTURE; CARBOXY TERMINAL SEQUENCE; CULTURE MEDIUM; GENE EXPRESSION REGULATION; NONHUMAN; PHOSPHATE METABOLISM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CROSS LINKING; PROTEIN DNA INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0030809030     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.20.6302-6310.1997     Document Type: Article

References (68)

1. Asayama, M., A. Yamamoto, and Y. Kobayashi. 1995. Dimer form of phosphorylated Spo0A, a transcriptional regulator, stimulates the spo0F transcription at the initiation of sporulation in Bacillus subtilis. J. Mol. Biol. 250:11-23.
2. Baikalov, I., I. Schröder, M. Kaczor-Grzeskowiak, K. Grzeskowiak, R. P. Gunsalus, and R. E. Dickerson. 1996. Structure of the Escherichia coli response regulator NarL. Biochemistry 35:11053-11061.
3. Birkey, S. M., G. Sun, P. J. Piggot, and F. M. Hulett. 1994. A pho regulon promoter induced under sporulation conditions. Gene 147:95-100.
4. Booksstein, C., C. W. Edwards, N. V. Kapp, and F. M. Hulett. 1990. The Bacillus subtilis 168 alkaline phosphatase III gene: the impact of a phoAIII mutation on total alkaline phosphatase synthesis. J. Bacteriol. 172:3730-3737.
5. Boucher, P. E., K. Murakami, A. Ishihama, and S. Stibitz. 1997. Nature of DNA binding and RNA polymerase interaction of the Bordetella pertussis BvgA transcriptional activator at the fha promoter. J. Bacteriol. 179:1755-1763.
6. Bourret, R. B., K. A. Borkovich, and M. I. Simon. 1991. Signal transduction pathways involving protein phosphorylation in prokyrotes. Annu. Rev. Biochem. 60:401-441.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
8. Brenowitz, M., D. Senear, and R. Kinston. 1996. DNase I footprint analysis of protein-DNA binding, p. 12.4.1-12.4.16. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 2. John Wiley & Sons, Inc., New York, N.Y.
9. Chesnut, R. S., C. Bookstein, and F. M. Hulett. 1991. Separate promoters direct expression of phoAIII, a member of the Bacillus subtilis alkaline phosphatase multigene family, during phosphate starvation and sporulation. Mol. Microbiol. 5:2181-2190.
10. Dahn, J. L., B. Y. Wei, and R. J. Kadner. 1997. Protein phosphorylation affects binding of the Escherichia coli transcription activator UhpA to the uhpT promoter. J. Biol. Chem. 272:1910-1919.
11. Deretic, V., H. H. J. Leveau, C. D. Mohr, and N. S. Hibler. 1992. In vitro phosphorylation of AlgR, a regulator of mucoidy in Pseudomonas aeruginosa, by a histidine protein kinase and effects of small phospho-donor molecules. Mol. Microbiol. 6:2761-2767.
12. + mutant of EnvZ (EnvZ.N347D), a bifunctional signal transducer of Escherichia coli. J. Biol. Chem. 271:1424-1429.
13. Eder, S., L. Shi, K. Jensen, K. Yamane, and F. M. Hulett. 1996. A Bacillus subtilis secreted phosphodiesterase/alkaline phosphatase is the product of a Pho regulon gene, phoD. Microbiology 142:2041-2047.
14. Engstrom, L. 1962. Incorporation of inorganic phosphate into alkaline phosphatase from Escherichia coli. Biochim. Biophys. Acta 56:606-609.
15. Feng, J., M. R. Atkinson, W. McCleary, J. B. Stock, B. L. Wanner, and A. J. Ninfa. 1992. Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli. J. Bacteriol. 174:6061-6070.
16. Fiedler, U., and V. Weiss. 1995. A common switch in activation of the response regulators NtrC and PhoB: phosphorylation induces dimerization of the receiver modules. EMBO J. 15:3696-3705.
17. Fisher, S., W. Jiang, B. L. Wanner, and C. T. Walsh. 1995. Cross-talk between the histidine protein kinase VanS and the response regulator PhoB-characterization and identification of a VanS domain that inhibits activation of PhoB. J. Biol. Chem. 270:23143-23149.
18. Hess, J. F., R. B. Bourett, and M. I. Simon. 1988. Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature (London) 336:139-143.
19. Hiratsu, K., A. Nakata, H. Shinagawa, and K. Makino. 1995. Autophosphorylation and activation of transcriptional activator PhoB of Escherichia coli by acetyl phosphate in vitro. Gene 161:7-10.
20. Hulett, F. M. 1993. Regulation of phosphorus metabolism, p. 229-235. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C.
21. Hulett, F. M. 1995. Complex phosphate regulation by sequential switches in Bacillus subtilis, p. 289-302. In J. A. Hoch and T. J. Silhavy (ed.), Two-component signal transduction. American Society for Microbiology, Washington, D.C.
22. Hulett, F. M. 1996. The signal transduction network for Pho regulation. Mol. Microbiol. 19:933-939.
23. Hulett, F. M. Unpublished data.
24. Hulett, F. M., C. Bookstein, and K. Jensen. 1990. Evidence for two structural genes for alkaline phosphatase in Bacillus subtilis. J. Bacteriol. 172:735-740.
25. Hulett, F. M., and K. Jenson. 1988. Critical roles of spo0A and spo0H in vegetative alkaline phosphatase production in Bacillus subtilis. J. Bacteriol. 170:3765-3768.
26. Hulett, F. M., E. E. Kim, C. Bookstein, N. Kapp, C. W. Edwards, and H. W. Wyckoff. 1991. Bacillus subtilis alkaline phosphatase III and IV. Cloning, sequencing, and comparisons of deduced amino acid sequence with Escherichia coli alkaline phosphatase three dimensional structure. J. Biol. Chem. 266:1077-1084.
27. Hulett, F. M., J. Lee, L. Shi, G. Sun, R. Chesnut, E. Sharkova, M. F. Duggan, and N. Kapp. 1994. Sequential action of two-component genetic switches regulates the PHO regulon in Bacillus subtilis. J. Bacteriol. 176:1348-1358.
28. Hulett, F. M., G. Sun, and W. Liu. 1994. The Pho regulon of Bacillus subtilis is regulated by sequential action of two genetic switches, p. 50-54. In A. Torriani-Gorini, E. Yogil, and S. Silver, (ed.), Phosphate in microorganisms: cellular and molecular biology. American Society for Microbiology, Washington, D.C.
29. Igo, M. M., A. J. Ninfa, J. B. Stock, and T. J. Silhavy. 1989. Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev. 3:598-605.
30. Kapp, N. V., C. W. Edwards, R. S. Chesnut, and F. M. Hulett. 1990. The Bacillus subtilis phoAIV gene: effects of in vitro inactivation on total alkaline phosphatase production. Gene 96:95-100.
31. Keener, J., and S. Kustu. 1988. Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: role of the conserved aminoterminal domain of NTRC. Proc. Natl. Acad. Sci. USA 85:4976-4980.
32. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
33. Lee, J. W., and F. M. Hulett. 1991. Nucleotide sequence of the phoP gene encoding PhoP, the response regulator of the phosphate regulon of Bacillus subtilis. Nucleic Acids Res. 20:5848.
34. Lois, A. F., M. Weinstein, G. Ditta, and D. R. Helinski. 1993. Autophosphorylation and phosphatase activities of the oxygen-sensing protein FixL of Rhizobium meliloti are coordinately regulated by oxygen. J. Biol. Chem. 268:4370-4375.
35. Lukat, G. S., W. R. McCleary, A. M. Stock, and J. B. Stock. 1992. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci. USA 89:718-722.
36. Makino, K., M. Amemura, T. Kawamoto, S. Kimura, H. Shinagawa, A. Nakata, and M. Suzuki. 1996. DNA binding of PhoB and its interaction with RNA polymerase. J. Mol. Biol. 259:15-26.
37. Makino, K., M. Amemura, S. Kim, A. Nakata, and H. Shinagawa. 1994. Mechanism of transcriptional activation of the phosphate regulon in Escherichia coli, p. 5-12. In A. Torriani-Gorini, E. Yagil, and S. Silver, (ed.), Phosphate in microorganisms: cellular and molecular biology. American Society for Microbiology, Washington, D.C.
38. Makino, K., H. Shinagawa, M. Amemura, T. Kawamoto, M. Yamada, and A. Nakata. 1989. Signal transduction in the phosphate regulon of Escherichia coli involves phosphotransfer between PhoR and PhoB proteins. J. Mol. Biol. 210:551-559.
39. Makino, K., H. Shinagawa, M. Amemura, S. Kimara, A. Nakata, and A. Ishihama. 1988. Regulation of the phosphate regulon of Escherichia coli. Activation of pstS transcription by PhoB protein in vitro. J. Mol. Biol. 203:85-95.
40. Manzara, T., P. Carrasco, and W. Gruissem. 1991. Developmental and organ-specific changes in promoter DNA-protein interactions in the tomato rbcS gene family. Plant Cell 3:1305-1316.
41. McCleary, W. R., J. B. Stock, and A. J. Ninfa. 1993. Is acetyl phosphate a global signal in Escherichia coli? J. Bacteriol. 175:2793-2798.
42. McCleary, W. 1996. The activation of PhoB by acetyl phosphate. Mol. Microbiol. 20:1155-1163.
43. Mizuno, T., and S. Mizushima. 1987. Isolation and characterization of deletion mutants of the ompR and envZ, regulatory genes for expression of the outer membrane proteins. J. Biochem. (Tokyo) 101:387-396.
44. Msadek, T., F. Kunst, and R. Rapoport. 1993. Two-component regulatory systems, p. 729-746. In A. L. Sonenshein, J. A. Hoch, and R. Losick, (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C.
45. Nakashima, K., K. Kanamaru, H. Aiba, and T. Mizuno. 1991. Signal transduction and osmoregulation in Escherichia coli: a novel type of mutation in the phosphorylation domain of the activator protein, OmpR, results in a defect in its phosphorylation-dependent DNA binding. J. Biol. Chem. 266: 10775-10780.
46. II, regulates the transcription of the glnALG operon in Escherichia coli. Proc. Natl. Acad. Sci. USA 83:5909-5913.
47. Ninfa, A. J., E. J. Ninfa, A. N. Lupas, A. Stock, B. Magasanik, and J. Stock. 1988. Cross talk between bacterial chemotaxis signal transduction proteins and regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. Proc. Natl. Acad. Sci. USA 83:7850-7854.
48. Ohlsen, K. L., J. K. Grimsley, and J. A. Hoch. 1994. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc. Natl. Sci. USA 91:1756-1760.
49. Perego, M., C. Hanstein, K. M. Welsh, T. Djavakhishvili, P. Glaser, and J. A. Hoch. 1994. Multiple protein aspartate phosphatases provide a mechanism for the interaction of diverse signals in the control of development in B. subtilis. Cell 79:1047-1055.
50. Porter, S. C., A. K. North, and S. Kustu. 1995. Mechanism of transcriptional activation by NtrC, p. 147-158. In J. A. Hoch and T. J. Silhavy (ed.), Two-component signal transduction. American Society for Microbiology, Washington, D.C.
51. Qi, Y., Y. Kobayashi, and F. M. Hulett. 1996. The pst operon of Bacillus subtilis has a phosphate-regulated promoter and is involved in phosphate transport but not in regulation of the Pho regulon. J. Bacteriol. 179:2534-2539.
52. Roggiani, M., and D. Dubnau. 1993. ComA, a phosphorylated response regulator protein of Bacillus subtilis, binds to the promoter region of srfA. J. Bactcriol. 175:3182-3187.
53. Russo, F., and T. J. Silhavy. 1991. EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J. Mol. Biol. 222:567-580.
54. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
55. Schwartz, L., and F. Lipmann. 1961. Phosphate incorporation into alkaline phosphatase of E. coli. Proc. Natl. Acad. Sci. USA 47:1996-2005.
56. Seki, T., H. Yoshikawa, H. Takahashi, and H. Saito. 1988. Nucleotide sequence of the Bacillus subtilis phoR gene. J. Bacteriol. 170:5935-5938.
57. Seki, T., H. Yoshikawa, H. Takahashi, and H. Saito. 1987. Cloning and nucleotide sequence of phoP, the regulatory gene for alkaline phosphatase and phosphodiesterase in Bacillus subtilis. J. Bacteriol. 169:2913-2916.
58. Shi, L., and F. M. Hulett. Unpublished data.
59. Soldo, B., V. Lazareric, M. Pagni, C. Mauël, and D. Karamata. 1995. Transcriptional regulation of teichuronic acid gene expression, p. 77. In Abstracts of the 8th International Conference on Bacilli.
60. Stock, J. B., M. G. Surette, and P. Park. 1995. Two-component signal transduction systems: structure-function relationship and mechanism of catalysis, p. 25-51. In J. A. Hoch and T. J. Silhavy (ed.), Two-component signal transduction. American Society for Microbiology, Washington, D.C.
61. Sun, G., E. Sharkova, R. Chesnut, S. Birkey, M. F. Duggan, A. Sorokin, P. Pujic, S. Dusko, and F. M. Hulett. 1996. Regulators of aerobic and anaerobic respiration in Bacillus subtilis. J. Bacteriol. 178:1374-1385.
62. Sun, G., S. M. Birkey, and F. M. Hulett. 1996. Three two-component signal-transduction systems interact for Pho regulation in Bacillus subtilis. Mol. Microbiol. 19:941-948.
63. Suzuki, M., and S. Brenner. 1995. Classification of multi-helical DNA-binding domains and application to predict the DBD structures of σ factor, LysR, OmpR/PhoB, CENP-B, Rap1, and XylS/Ada/AraC. FEBS Lett. 372:215-221.
64. Wanner, B. L., and M. R. Wilmes-Riesenberg. 1992. Involvement of phosphotransacetylase, acetyl kinase and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J. Bacteriol. 174:2124-2130.
65. Wanner, B. L. 1996. Phosphate assimilation and control of the phosphate regulon, p. 1357-1381. In F. C. Neidhart, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, D.C.
66. Wyman, C., I. Rombel, A. North, C. Bustamante, and S. Kustu. 1997. Unusual oligomerization required for activity of NtrC, a bacterial enhancer-binding protein. Science 275:1658-1661.
67. Yamada, M., K. Makino, H. Shinagawa, and A. Nakata. 1990. Regulation of phosphate regulon of Escherichia coli: properties of phoR deletion mutant and subcellular localization of PhoR protein. Mol. Gen. Genet. 220:366-372.
68. Yang, X. F., C. M. Kang, M. S. Broady, and C. W. Price. 1996. Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcriptional factor. Gene Dev. 10:2265-2275.