Dimer-induced signal progation in Spo0A

Molecular Microbiology

Volumn 53, Issue 3, 2004, Pages 829-842

  Muchova K ^a   Lewis, R J ^b,c   Perecko D ^a   Brannigan, J A ^b   Ladds, J C ^b   Leech, A ^b   Wilkinson, A J ^b   Barak I ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b UNIVERSITY OF YORK   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; DIMER; MUTANT PROTEIN; PHENYLALANINE; PHOSPHORAMIDIC ACID; PROTEIN SPO0A; REGULATOR PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL STRAIN; DIMERIZATION; DNA BINDING; GEL FILTRATION CHROMATOGRAPHY; GEL MOBILITY SHIFT ASSAY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SPOROGENESIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; DIMERIZATION; DNA PRIMERS; ETHYL METHANESULFONATE; MODELS, MOLECULAR; MUTAGENESIS; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PLASMIDS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SPORES, BACTERIAL; TRANSCRIPTION FACTORS; X-RAY DIFFRACTION;

BACILLI; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 3843050402     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04171.x     Document Type: Article

References (50)

1. Allen, M.P., Zumbrennen, K.B., and McCleary, W.R. (2001) Genetic evidence that the α5 helix of the receiver domain of PhoB is involved in interdomain interactions. J Bacteriol 183: 2204-2211.
2. Asayama, M., Yamamoto, A., and Kobayashi, Y. (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.
3. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.O., Seidmann, J.S., Smith, J., and Struhl, K. (1987) Current Protocols in Molecular Biology. New York: Wiley.
4. Backman, K., Ptashne, M., and Gilbert, A.W. (1976) Construction of plasmids carrying the cl gene of bacteriophage lambda. Proc Natl Acad Sci USA 73: 4174-4178.
5. Birck, C., Mourey, L., Gouet, P., Fabry, B., Schumacher, J., Rousseau, P., et al. (1999) Conformational changes induced by phosphorylation of the FixJ receiver domain. Structure 7: 1505-1515.
6. Brown, D.P., Ganova-Raeva, L., Green, B.D., Wilkinson, S.R., Young, M., and Youngman, P. (1994) Characterization of Spo0A homologs in diverse Bacillus and Clostridium species identifies a probable DNA-binding domain. Mol Microbiol 14: 411-426.
7. 32P] phosphoramidate for use as a low molecular weight phosphodonor reagent. Anal Biochem 283: 222-227.
8. Cervin, M.A., and Spiegelman, G.B. (1999) The Spo0A sof mutations reveal regions of the regulatory domain that interact with a sensor kinase and RNA polymerase. Mol Microbiol 31: 597-607.
9. 75 in domain interaction in the Bacillus subtilis response regulator Spo0A. J Biol Chem 275: 22025-22030.
10. Cho, H.S., Pelton, J.G., Yan, D., Kustu, S., and Wemmer, D.E. (2001) Phosphoaspartates in bacterial signal transduction. Curr Opin Struct Biol 11: 679-684.
11. Chung, J.D., Stephanopoulos, G., Ireton, K., and Grossman, A.D. (1994) Gene expression in single cells of Bacillus subtilis: evidence that a threshold mechanism controls the initiation of sporulation. J Bacteriol 176: 1977-1984.
12. Da Re, S., Schumacher, J., Rousseau, P., Fourment, J., Ebel, C., and Kahn, D. (1999) Phosphorylation-induced dimerization of the FixJ receiver domain. Mol Microbiol 34: 504-511.
13. Djordjevic, S., Goudreau, P.N., Xu, Q., Stock, A.M., and West, A.H. (1998) Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. Proc Natl Acad Sci USA 95: 1381-1386.
14. Ellison, D.W., and McCleary, W.R. (2000) The unphosphorylated receiver domain of PhoB silences the activity of its output domain. J Bacteriol 182: 6592-6597.
15. Fawcett, P., Eichenberger, P., Losick, R., and Youngman, P. (2000) The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 97: 8063-8068.
16. Florek, P., Muchová, K., and Barák, I. (2002) Truncated SpoOA transcription activities in Bacillus subtilis. Biología (Bratislava) 57: 805-811.
17. 3-activated Spo0F reveals the conformational switch in a phosphorelay system. J Mol Biol 331: 245-254.
18. Grimsley, J.K., Tjalkens, R.B., Strauch, M.A., Bird, T.H., Spiegelman, G.B., Hostomsky, Z., et al. (1994) Subunit composition and domain structure of the Spo0A sporulation transcription factor of Bacillus subtilis. J Biol Chem 269: 16977-16982.
19. Harwood, C.R., and Cutting, S.M. (eds) (1990) Molecular Biological Methods for Bacillus. Chichester: John Wiley and Sons.
20. Hastings, C.A., Lee, S.Y., Cho, H.S., Van, D., Kustu, S., and Wemmer, D.E. (2003) High-resolution structure of the beryllofluoride-activated NtrC receiver domain. Biochemistry 42: 9081-9090.
21. Ireton, K., Rudner, D.Z., Siranosian, K.J., and Grossman, A.D. (1993) Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. Genes Dev 7: 283-294.
22. Jiang, M., Shao, W., Perego, M., and Hoch, J.A. (2000) Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol 38: 535-542.
23. Kormanec, J., and Farkasovsky, M. (1993) Simple and reliable determination of radioactive precursor-incorporation into nucleic acids in vitro. Biotechniques 15: 400.
24. Ladds, J., Muchová, K., Blaskovic, D., Lewis, R.J., Brannigan, J.A., Wilkinson, A.J., and Barák, I. (2003) The response regulator Spo0A from Bacillus subtilis is efficiently phosphorylated in Escherichia coli. FEMS Microbiol Lett 223: 153-157.
25. Laue, T.M., Shah, B.D., Ridgeway, T.M., and Pelletier, S.L. (1992) Computer aided interpretation of analytical sedimentation data for proteins. In Analytical Ultracentrifugation in Biochemistry and Polymer Science. Harding, S.E., Rowe, A.J., and Horton, J.C. (eds). Cambridge: Royal Society of Chemistry, pp. 90-125.
26. Lee, S.Y., Cho, H.S., Pelton, J.G., Yan, D., Henderson, R.K., King, D.S., et al. (2001) Crystal structure of an activated response regulator bound to its target. Nature Struct Biol 8: 52-56.
27. Lewis, R.J., Brannigan, J.A., Muchová, K., Barák, I., and Wilkinson, A.J. (1999) Phosphorylated aspartate in the structure of a response regulator protein. J Mol Biol 294: 9-15.
28. Lewis, R.J., Muchová, K., Brannigan, J.A., Barák, I., Leonard, G., and Wilkinson, A.J. (2000a) Domain swapping in the sporulation response regulator, Spo0A. J Mol Biol 297: 757-770.
29. Lewis, R.J., Krzwyda, S., Brannigan, J.A., Turkenburg, J.P., Muchová, K., Dodson, E.J., et al. (2000b) The transactivation domain of the sporulation response regulator SpoOA, revealed by X-ray crystallography. Mol Microbiol 38: 198-212.
30. Lewis, R.J., Brannigan, J.A., Barák, I., and Wilkinson, A.J. (2001) Lessons and questions from the structure of the SpoOA activation domain: response. Trends Microbiol 9: 150-151.
31. Lewis, R.J., Scott, D.J., Brannigan, J.A., Ladds, J.C., Cervin, M.A., Spiegelman, G.B., et al. (2002) Dimer formation and transcription activation in the sporulation response regulator Spo0A. J Mol Biol 316: 235-245.
32. McEvoy, M.M., Hausrath, A.C., Randolph, G.B., Remington, S.J., and Dahlquist, F.W. (1998) Two binding modes reveal flexibility in kinase/response regulator interactions in the bacterial chemotaxis pathway. Proc Natl Acad Sci USA 95: 7333-7338.
33. Madhusudan, Zapf, J., Hoch, J.A., Whiteley, J.M., Xuong, N.H., and Varughese, K.I. (1997) A response regulatory protein with the site of phosphorylation blocked by an arginine interaction: crystal structure of Spo0F from Bacillus subtilis. Biochemistry 36: 12739-12745.
34. Muchová, K., Lewis, R.J., Brannigan, J.A., Offen, W.A., Brown, D.P., Barák, I., et al. (1999) Crystallisation of the regulatory and effector domains of the key sporulation response regulator Spo0A. Acta Crystallogr D55: 671-676.
35. Olmedo, G., Ninfa, E.G., Stock, J., and Youngman, P. (1990) Novel mutations that alter regulation of sporulation in Bacillus subtilis: evidence that phosphorylation of regulatory protein SpoOA controls the initiation of sporulation. J Mol Biol 215: 359-372.
36. - selects between alternate dimeric states of the receiver domain, FASEB J 16: 1964-1966.
37. Perego, M., Wu, J.-J., Spiegelman, G.B., and Hoch, J.A. (1991) Mutational dissociation of the positive and negative regulatory properties of the Spo0A sporulation transcription factor of Bacillus subtilis. Gene 100: 207-212.
38. Saito, K., Ito, E., Hosono, K., Nakamura, K., Imai, K., Iizuka, T., et al. (2003) The uncoupling of oxygen sensing, phosphorylation signalling and transcriptional activation in oxygen sensor FixL and FixJ mutants. Mol Microbiol 48: 373-383.
39. Schmeisser, F., Brannigan, J.A., Lewis, R.J., Wilkinson, A.J., Youngman, P., and Barák, I. (2000) A new mutation in spo0A with intragenic suppressors in the effector domain. FEMS Microbiol Lett 185: 123-128.
40. Schuck, P. (2000) Size distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78: 1606-1619.
41. Spiegelman, G.B., Van Hoy, B., Perego, M., Day, J., Trach, K., and Hoch, J.A. (1990) Structural alterations in the Bacillus subtilis Spo0A regulatory protein which suppresses mutations at several spo0 loci. J Bacteriol 172: 5011-5019.
42. Spiegelman, G.B., Bird, T.H., and Voon, V. (1995) Transcription regulation by the Spo0A protein of Bacillus subtilis. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington, DC: American Society for Microbiology Press, pp. 159-179.
43. Strauch, M.A., Webb, V., Spiegelman, G.B., and Hoch, J.A. (1990) The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Proc Natl Acad Sci USA 87: 1801-1805.
44. Trach, K., Burbulys, D., Strauch, M.A., Wu, J.-J., Dhillion, N., Jonas, R., et al. (1991) Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay. Res Microbiol 142: 815-823.
45. Tzeng, Y., and Hoch, J.A. (1997) Molecular recognition in signal transduction: the interaction surfaces of the SpoOF response regulator with its cognate phosphorelay proteins revealed by alanine scanning mutagenesis. J Mol Biol 272: 200-212.
46. Vanish-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.
47. Youngman, P. (1990) Use of transposons and integrational vectors for mutagenesis and construction of gene fusions in Bacillus species. In Molecular Biological Methods for Bacillus. Harwood, C.R., and Cutting, S.M. (eds). Chichester: John Wiley & Sons, pp. 221-266.
48. Zapf, J.W., Hoch, J.A., and Whiteley, J.M. (1996) A phosphotransferase activity of the Bacillus subtilis sporulation protein SpoOF that employs phosphoramidate substrates. Biochemistry 35: 2926-2933.
49. Zapf, J., Madhusudan, Sen, U., Hoch, J.A., and Varughese, K.I. (2000) A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 8: 851-862.
50. Zhao, H., Msadek, T., Zapf, J., Madhusudan, Hoch, J.A., and Varughese, K.I. (2002) DNA complex structure of the key transcription factor initiating development in sporulating bacteria. Structure 10: 1041-1050.