The atypical hybrid histidine protein kinase RodK in myxococcus xanthus: Spatial proximity supersedes kinetic preference in phosphotransfer reactions

Journal of Bacteriology

Volumn 191, Issue 6, 2009, Pages 1765-1776

  Wegener Feldbrügge, Sigrun ^a   Søgaard Andersen, Lotte ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PHOSPHATE; PROTEIN HISTIDINE KINASE; PROTEIN RODK; PROTEIN ROKA; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE;

ARTICLE; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FRUITING BODY; GENOME SIZE; MYXOCOCCUS XANTHUS; NONHUMAN; PHOSPHATE TRANSPORT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

MYXOCOCCUS XANTHUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; KINETICS; MOLECULAR SEQUENCE DATA; MYXOCOCCUS XANTHUS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

EID: 63049131978     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01405-08     Document Type: Article

References (48)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Meyers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-110.
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. Biondi, E. G., S. J. Reisinger, J. M. Skerker, M. Arif, B. S. Perchuk, K. R. Ryan, and M. T. Laub. 2006. Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444:899-904.
4. Bourret, R. B. 2008. Signal transduction meets systems biology: deciphering specificity determinants for protein-protein interactions. Mol. Microbiol. 69:1336-1340.
5. Burbulys, D., K. A. Trach, and J. A. Hoch. 1991. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64:545-552.
6. Cho, K., and D. R. Zusman. 1999. Sporulation timing in Myxococcus xanthus is controlled by the espAB locus. Mol. Microbiol. 34:714-725.
7. Dworkin, M. 1996. Recent advances in the social and developmental biology of the myxobacteria. Microbiol. Rev. 60:70-102.
8. Ellehauge, E., M. NØrregaard-Madsen, and L. SØgaard-Andersen. 1998. The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in M. xanthus development. Mol. Microbiol. 30:807-817.
9. Galperin, M. 2005. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 5:35.
10. Galperin, M. Y. 2006. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol. 188:4169-4182.
11. Georgellis, D., A. S. Lynch, and E. C. C. Lin. 1997. In vitro phosphorylation studv of the Arc two-component signal transduction system of Escherichia coli.J. Bacteriol. 179:5429-5435.
12. Goodman, A. L., B. Kulasekara, A. Rietsch, D. Boyd, R. S. Smith, and S. Lory. 2004. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aemginosa. Dev. Cell 7:745-754.
13. Henke, J. M., and B. L. Bassler. 2004. Three parallel quorum-sensing systems regulate gene expression in Vibrio haiveyi. J. Bacteriol. 186:6902-6914.
14. Higgs, P. L, K. Cho, D. E. Whirworth, L. S. Evans, and D. R. Zusman. 2005. Four unusual two-component signal transduction homologs, RedC to RedF, are necessary for timely development in Myxococcus xanthus. J. Bacteriol. 187:8191-8195.
15. Hodgkin, J., and D. Kaiser. 1977. Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc. Natl. Acad. Sei. USA 74:2938-2942.
16. Hsu, J. L., H. C. Chen, H. L. Peng, and H. Y. Chang. 2008. Characterization of the histidine-containing phosphotransfer protein B-mediated multistep phosphorelay system in Pseudomonas aeruginosa PAOl. J. Biol. Chem. 283: 9933-9944.
17. Jiang, M., W. Shao, M. Perego, and J. A. Hoch. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus suhtilis. MoL. Microbiol. 38:535-542.
18. Julien, B., A. D. Kaiser, and A. Garza. 2000. Spatial control of cell differentiation in Myxococcus xanthus. Proc. Natl. Acad. Sei. USA 97:9098-9103.
19. Kaiser, D. 1979. Social gliding is correlated with the presence of piLi in Myxococcus xanthus. Proc. Natl. Acad. SCi. USA 76:5952-5956.
20. Kiil, K., J. B. Ferchaud, C. David, T. T. Binnewies, H. Wu, T. Sicheritz-Ponten, H. Willenbrock, and D. W. Ussery. 2005. Genome update: distribution of two-component transduction svstems in 250 bacterial genomes. Microbiology 151:3447-3452.
21. Kumar, A., J. C. Toledo, R. P. Patel, J. R. Lancaster, Jr., and A. J. Steyn. 2007. Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl. Acad. Sci. USA 104:11568-11573.
22. Laskowski, M. A., and B. I. Kazmierczak. 2006. Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infect. Immun. 74:4462-4473.
23. Laub, M. T., and M. Goulian. 2007. Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41:121-145.
24. Lee, B., P. I. Higgs, D. R. Zusman, and K. Cho. 2005. EspC is involved in controlling the timing of development in Myxococcus xanthus. J. Bacteriol. 187:5029-5031.
25. Letunic, I., R. R. Copley, S. Schmidt, F. D. Ciccarelli, T. Doerks, J. Schultz, C. P. Ponting, and P. Bork. 2004. SMART 4.0: towards genomic data integration. Nucleic Acids Res. 32:D142-D144.
26. Lutz, R., and H. Bujard. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/ 11-12 regulatory elements. Nucleic Acids Res. 25:1203-1210.
27. Maeda, S., C. Sugita, M. Sugita, and T. Omata. 2006. A new class of signal transducer in His-Asp phosphorelay systems. J. Biol. Chem. 281:37868-37876.
28. Mok, K. C, N. S. Wingreen, and B. L. Bassler. 2003. Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J. 22:870-881.
29. O'Connor, K. A., and D. R. Zusman. 1991. Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J. Bacteriol. 173:3318-3333.
30. Ogawa, M., S. Fujitani, X. Mao, S. Inouye, and T. Komano. 1996. FruA, a putative transcription factor essential for the development of Myxococcus xanthus. Mol. Microbiol. 22:757-767.
31. Overgaard, M., S. Wegener-Feldbrügge, and L. SØgaard- Andersen. 2006. The orphan response regulator DigR is required for synthesis of extracellular matrix fibrils in Myxococcus xanthus. J. Bacteriol. 188:4384-394.
32. Posas, F., and H. Saito. 1998. Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J. 17:1385-1394.
33. Rasmussen, A. A-, S. L. Porter, J. P. Armitage, and L. Søgaard-Andersen. 2005. Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase during fruiting body morphogenesis in Myxococcus xanthus. Mol. Microbiol. 56:1358-1372.
34. Rasmussen, A. A,, and L. SØgaard-Andersen. 2003. TodK, a putative histidine protein kinase, regulates timing of fruiting body morphogenesis in Myxococcus xanthus. J. Bacteriol. 185:5452-5464.
35. Rasmussen, A. A., S. Wegener-Feldbrügge, S. L. Porter, J. P. Armitage, and L. Søgaard-Andersen. 2006. Four signalling domains in the hybrid histidine protein kinase RodK of Myxococcus xanthus are required for activity. Mol. Microbiol. 60:525-534.
36. Robinson, V. L,, D. R. Buckler, and A. M. Stock. 2000. A tale of two components: a novel kinase and a regulatory switch. Nat. Struct. Biol. 7:626-633.
37. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY.
38. Shi, X., S. Wegener-Feldbriigge, S. Huntley, N. Hamann, R. Hedderich, and L. SØgaard-Andersen. 2008. Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus. J. Bacteriol. 190:613-624.
39. Shimkets, L. J., and D. Kaiser. 1982. Induction of coordinated movement of Myxococcus xanthus cells. J. Bacteriol. 152:451-461.
40. Skerker, J. M., M. S. Prasol, B. S. Perchuk, E. G. Biondi, and M. T. Laub. 2005. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol. 3:e334.
41. SØgaard-Andersen, L., F. J. Slack, H. Kimsey, and D. Kaiser. 1996. Intercellular C-signaling in Myxococcus xanthus involves a branched signal transduction pathway. Genes Dev. 10:740-754.
42. Stock, A. M., V. L. Robinson, and P. N. Goudreau. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183-215.
43. Takeda, S., Y. Fujisawa, M. Matsubara, H. Aiba, and T. Mizuno. 2001. A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC to YojN to RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol. Microbiol. 40:440-450.
44. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
45. Uhl, M. A., and J. F. Miller. 1996. Central role of the BvgS receiver as a phosphorylated intermediate in a complex two-component regulatory phosphorelay. J. Biol. Chem. 271:33176-33180.
46. Welch, M., K. Oosawa, S. Aizawa, and M. Eisenbach. 1993. Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc. Natl. Acad. Sci. USA 90:8787-8791.
47. Whitworth, D. E., and P. J. A. Cock. 2008. Two-component systems of the myxobacteria: structure, diversity and evolutionary relationships. Microbiology 154:360-372.
48. Yamamoto, K, K. Hirao, T. Oshima, H. Aiba, R. Utsumi, and A. Ishihama. 2005. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280:1448-1456.