Summary of useful methods for two-component system research

Current Opinion in Microbiology

Volumn 13, Issue 2, 2010, Pages 246-252

  Scharf, Birgit E ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATE; PROTEIN HISTIDINE KINASE;

BACTERIAL GENOME; CHEMOTAXIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MEDICAL RESEARCH; NITROGEN FIXATION; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; FLUORESCENCE RESONANCE ENERGY TRANSFER; MUTAGENESIS; PROTEIN KINASES; RESEARCH; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS);

EID: 77950295912     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2010.01.006     Document Type: Review

References (90)

1. Wuichet K., Cantwell B.J., and Zhulin I.B. Evolution and phyletic distribution of two-component signal transduction systems. Curr Opin Microbiol (2010) 13
2. Mizuno T. Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci Biotechnol Biochem 69 12 (2005) 2263-2276
3. Loomis W.F., Shaulsky G., and Wang N. Histidine kinases in signal transduction pathways of eukaryotes. J Cell Sci 110 Pt 10 (1997) 1141-1145
4. Kirby J.R. Chemotaxis-like regulatory systems: unique roles in diverse bacteria. Annu Rev Microbiol 63 (2009) 45-59
5. Scharf B.E., Aldridge P.D., Kirby J.R., and Crane B.R. Upward mobility and alternative lifestyles: a report from the 10th biennial meeting on Bacterial Locomotion and Signal Transduction. Mol Microbiol 73 1 (2009) 5-19 PMCID: 2724751
6. Ninfa A.J., and Magasanik B. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci U S A. 83 16 (1986) 5909-5913 PMCID: 386406
7. Hess J.F., Oosawa K., Matsumura P., and Simon M.I. Protein phosphorylation is involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 84 21 (1987) 7609-7613 PMCID: 299349
8. Gao R., and Stock A.M. Biological insights from structures of two-component proteins. Annu Rev Microbiol 63 (2009) 133-154
9. Simon MI, Crane, B.R., Crane, A., editor. Two-Component Signaling Systems, Part A Methods Enzymol 2007, 422.
10. Simon MI, Crane, B.R., Crane, A., editor. Two-Component Signaling Systems, Part B Methods Enzymol 2007, 423.
11. Hess J.F., Bourret R.B., and Simon M.I. Phosphorylation assays for proteins of the two-component regulatory system controlling chemotaxis in Escherichia coli. Methods Enzymol 200 (1991) 188-204. The first collation of TCS phosphorylation assays.
12. Conley M.P., Berg H.C., Tawa P., Stewart R.C., Ellefson D.D., and Wolfe A.J. pH dependence of CheA autophosphorylation in Escherichia coli. J Bacteriol 176 13 (1994) 3870-3877 PMCID: 205583
13. Noriega C.E., Schmidt R., Gray M.J., Chen L.L., and Stewart V. Autophosphorylation and dephosphorylation by soluble forms of the nitrate-responsive sensors NarX and NarQ from Escherichia coli K-12. J Bacteriol 190 11 (2008) 3869-3876 PMCID: 2395026
14. Tawa P., and Stewart R.C. Kinetics of CheA autophosphorylation and dephosphorylation reactions. Biochemistry 33 25 (1994) 7917-7924
15. Hess J.F., Oosawa K., Kaplan N., and Simon M.I. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53 1 (1988) 79-87
16. Dutta R., and Inouye M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25 1 (2000) 24-28
17. Hu X., Machius M., and Yang W. Monovalent cation dependence and preference of GHKL ATPases and kinases. FEBS Lett 544 1-3 (2003) 268-273
18. Lukat G.S., Stock A.M., and Stock J.B. Divalent metal ion binding to the CheY protein and its significance to phosphotransfer in bacterial chemotaxis. Biochemistry 29 23 (1990) 5436-5442
19. McCleary W.R., and Zusman D.R. Purification and characterization of the Myxococcus xanthus FrzE protein shows that it has autophosphorylation activity. J Bacteriol 172 12 (1990) 6661-6668 PMCID: 210777
20. Needham J.V., Chen T.Y., and Falke J.J. Novel ion specificity of a carboxylate cluster Mg(II) binding site: strong charge selectivity and weak size selectivity. Biochemistry 32 13 (1993) 3363-3367
21. Feher V.A., Zapf J.W., Hoch J.A., Dahlquist F.W., Whiteley J.M., and Cavanagh J. 1H, 15N, and 13C backbone chemical shift assignments, secondary structure, and magnesium-binding characteristics of the Bacillus subtilis response regulator, Spo0F, determined by heteronuclear high-resolution NMR. Protein Sci 4 9 (1995) 1801-1814 PMCID: 2143210
22. Ulrich L.E., Koonin E.V., and Zhulin I.B. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol 13 2 (2005) 52-56
23. Aiba H., Mizuno T., and Mizushima S. Transfer of phosphoryl group between two regulatory proteins involved in osmoregulatory expression of the ompF and ompC genes in Escherichia coli. J Biol Chem 264 15 (1989) 8563-8567
24. Chamnongpol S., and Groisman E.A. Acetyl phosphate-dependent activation of a mutant PhoP response regulator that functions independently of its cognate sensor kinase. J Mol Biol 300 2 (2000) 291-305
25. Borkovich K.A., and Simon M.I. The dynamics of protein phosphorylation in bacterial chemotaxis. Cell 63 6 (1990) 1339-1348
26. Chervitz S.A., and Falke J.J. Lock on/off disulfides identify the transmembrane signaling helix of the aspartate receptor. J Biol Chem 270 41 (1995) 24043-24053
27. Lee G.F., Burrows G.G., Lebert M.R., Dutton D.P., and Hazelbauer G.L. Deducing the organization of a transmembrane domain by disulfide cross-linking. The bacterial chemoreceptor. Trg J Biol Chem 269 47 (1994) 29920-29927
28. Ma P., Yuille H.M., Blessie V., Gohring N., Igloi Z., Nishiguchi K., et al. Expression, purification and activities of the entire family of intact membrane sensor kinases from Enterococcus faecalis. Mol Membr Biol 25 6-7 (2008) 449-473
29. Martin M., Albanesi D., Alzari P.M., and de Mendoza D. Functional in vitro assembly of the integral membrane bacterial thermosensor DesK. Protein Expr Purif 66 1 (2009) 39-45
30. Civjan N.R., Bayburt T.H., Schuler M.A., and Sligar S.G. Direct solubilization of heterologously expressed membrane proteins by incorporation into nanoscale lipid bilayers. Biotechniques 35 3 (2003) 556-60, 62-3
31. Boldog T., Grimme S., Li M., Sligar S.G., and Hazelbauer G.L. Nanodiscs separate chemoreceptor oligomeric states and reveal their signaling properties. Proc Natl Acad Sci U S A 103 31 (2006) 11509-11514. PMCID: 1544200. Application of the Nanodisc technology for the analysis of bacterial chemoreceptor signaling.
32. Boldog T., Li M., and Hazelbauer G.L. Using Nanodiscs to create water-soluble transmembrane chemoreceptors inserted in lipid bilayers. Methods Enzymol 423 (2007) 317-335
33. Appleman J.A., Chen L.L., and Stewart V. Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases. J Bacteriol 185 16 (2003) 4872-4882 PMCID: 166472
34. Xu Q., Black W.P., Ward S.M., and Yang Z. Nitrate-dependent activation of the Dif signaling pathway of Myxococcus xanthus mediated by a NarX-DifA interspecies chimera. J Bacteriol 187 18 (2005) 6410-6418 PMCID: 1236652
35. Ward S.M., Delgado A., Gunsalus R.P., and Manson M.D. A NarX-Tar chimera mediates repellent chemotaxis to nitrate and nitrite. Mol Microbiol 44 3 (2002) 709-719
36. Yoshida T., Phadtare S., and Inouye M. The design and development of Tar-EnvZ chimeric receptors. Methods Enzymol 423 (2007) 166-183
37. Utsumi R., Brissette R.E., Rampersaud A., Forst S.A., Oosawa K., and Inouye M. Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate. Science 245 4923 (1989) 1246-1249. The first study using chimeric receptors proteins to analyze gene expression.
38. Möglich A., Ayers R.A., and Moffat K. Design and signaling mechanism of light-regulated histidine kinases. J Mol Biol 385 5 (2009) 1433-1444. This report describes functional chimeric fusions between photo- and chemosensors.
39. Draheim R.R., Bormans A.F., Lai R.Z., and Manson M.D. Tuning a bacterial chemoreceptor with protein-membrane interactions. Biochemistry 45 49 (2006) 14655-14664
40. Lukat G.S., McCleary W.R., Stock A.M., and Stock J.B. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci U S A 89 2 (1992) 718-722
41. Silversmith R.E., Appleby J.L., and Bourret R.B. Catalytic mechanism of phosphorylation and dephosphorylation of CheY: kinetic characterization of imidazole phosphates as phosphodonors and the role of acid catalysis. Biochemistry 36 48 (1997) 14965-14974
42. Mayover T.L., Halkides C.J., and Stewart R.C. Kinetic characterization of CheY phosphorylation reactions: comparison of P-CheA and small-molecule phosphodonors. Biochemistry 38 8 (1999) 2259-2271
43. Zapf J.W., Hoch J.A., and Whiteley J.M. A phosphotransferase activity of the Bacillus subtilis sporulation protein Spo0F that employs phosphoramidate substrates. Biochemistry 35 9 (1996) 2926-2933
44. Thomason P.A., Traynor D., Cavet G., Chang W.T., Harwood A.J., and Kay R.R. An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium. EMBO J 17 10 (1998) 2838-2845 PMCID: 1170624
45. Stadtman E.R. Preparation and Assay of Acetyl Phosphate. Methods Enzymol 3 (1957) 228-231
46. Quon K.C., Marczynski G.T., and Shapiro L. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84 1 (1996) 83-93
47. Sheridan R.C., McCullough J.F., and Wakefield Z.T. Phosphoramidic acid and its salts. Inorg Synth (1971) 13
48. 32P]phosphoramidate for use as a low molecular weight phosphodonor reagent. Anal Biochem 283 2 (2000) 222-227
49. Rathlev T., and Rosenberg T. Non-enzymic formation and rupture of phosphorus to nitrogen linkages in phosphoramido derivatives. Arch Biochem Biophys 65 (1956) 319-339
50. Laub M.T., Biondi E.G., and Skerker J.M. Phosphotransfer profiling: systematic mapping of two-component signal transduction pathways and phosphorelays. Methods Enzymol 423 (2007) 531-548. A detailed guide to system-level phosphotransfer profiling.
51. Ulrich L.E., and Zhulin I.B. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res (2009). A comprehensive electronic catalogue of microbial signal transduction proteins.
52. Laub M.T., and Goulian M. Specificity in two-component signal transduction pathways. Annu Rev Genet 41 (2007) 121-145
53. Ferre A., De La Mora J., Ballado T., Camarena L., and Dreyfus G. Biochemical study of multiple CheY response regulators of the chemotactic pathway of Rhodobacter sphaeroides. J Bacteriol 186 15 (2004) 5172-5177 PMCID: 451638
54. Boesch K.C., Silversmith R.E., and Bourret R.B. Isolation and characterization of nonchemotactic CheZ mutants of Escherichia coli. J Bacteriol 182 12 (2000) 3544-3552 PMCID: 101953
55. Silversmith R.E., Smith J.G., Guanga G.P., Les J.T., and Bourret R.B. Alteration of a nonconserved active site residue in the chemotaxis response regulator CheY affects phosphorylation and interaction with CheZ. J Biol Chem 276 21 (2001) 18478-18484
56. Silversmith R.E., Levin M.D., Schilling E., and Bourret R.B. Kinetic characterization of catalysis by the chemotaxis phosphatase CheZ. Modulation of activity by the phosphorylated CheY substrate. J Biol Chem 283 2 (2008) 756-765. Non-radioactive phosphorylation assay in microtiter formate
57. Barbieri C.M., and Stock A.M. Universally applicable methods for monitoring response regulator aspartate phosphorylation both in vitro and in vivo using Phos-tag-based reagents. Anal Biochem 376 1 (2008) 73-82. PMCID: 2504525. Non-radioactive phosphorylation assay
58. Yan D., Cho H.S., Hastings C.A., Igo M.M., Lee S.Y., Pelton J.G., et al. Beryllofluoride mimics phosphorylation of NtrC and other bacterial response regulators. Proc Natl Acad Sci U S A 96 26 (1999) 14789-14794. This study established the use of beryllofluoride modification to create stable activated response regulators.
59. Saxl R.L., Anand G.S., and Stock A.M. Synthesis and biochemical characterization of a phosphorylated analogue of the response regulator CheB. Biochemistry 40 43 (2001) 12896-12903
60. Silversmith R.E., and Bourret R.B. Synthesis and characterization of a stable analog of the phosphorylated form of the chemotaxis protein CheY. Protein Eng 11 3 (1998) 205-212
61. Halkides C.J., Zhu X., Phillion D.P., Matsumura P., and Dahlquist F.W. Synthesis and biochemical characterization of an analogue of CheY-phosphate, a signal transduction protein in bacterial chemotaxis. Biochemistry 37 39 (1998) 13674-13680
62. Wolanin P.M., Webre D.J., and Stock J.B. Mechanism of phosphatase activity in the chemotaxis response regulator CheY. Biochemistry 42 47 (2003) 14075-14082
63. Bourret R.B., Hess J.F., and Simon M.I. Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc Natl Acad Sci U S A 87 1 (1990) 41-45
64. Scharf B.E., Fahrner K.A., Turner L., and Berg H.C. Control of direction of flagellar rotation in bacterial chemotaxis. Proc Natl Acad Sci U S A 95 1 (1998) 201-206
65. Smith J.G., Latiolais J.A., Guanga G.P., Citineni S., Silversmith R.E., and Bourret R.B. Investigation of the role of electrostatic charge in activation of the Escherichia coli response regulator CheY. J Bacteriol 185 21 (2003) 6385-6391 PMCID: 219398
66. Smith J.G., Latiolais J.A., Guanga G.P., Pennington J.D., Silversmith R.E., and Bourret R.B. A search for amino acid substitutions that universally activate response regulators. Mol Microbiol 51 3 (2004) 887-901
67. Moore J.B., Shiau S.P., and Reitzer L.J. Alterations of highly conserved residues in the regulatory domain of nitrogen regulator I (NtrC) of Escherichia coli. J Bacteriol 175 9 (1993) 2692-2701 PMCID: 204572
68. Klose K.E., Weiss D.S., and Kustu S. Glutamate at the site of phosphorylation of nitrogen-regulatory protein NTRC mimics aspartyl-phosphate and activates the protein. J Mol Biol 232 1 (1993) 67-78
69. Lan C.Y., and Igo M.M. Differential expression of the OmpF and OmpC porin proteins in Escherichia coli K-12 depends upon the level of active OmpR. J Bacteriol 180 1 (1998) 171-174 PMCID: 106865
70. Sourjik V., and Berg H.C. Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37 4 (2000) 740-751
71. Wadhams G.H., Martin A.C., and Armitage J.P. Identification and localization of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides. Mol Microbiol 36 6 (2000) 1222-1233
72. Meier V.M., and Scharf B.E. Cellular localization of predicted transmembrane and soluble chemoreceptors in Sinorhizobium meliloti. J Bacteriol 191 18 (2009) 5724-5733 PMCID: 2737976
73. Güvener Z.T., Tifrea D.F., and Harwood C.S. Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol Microbiol 61 1 (2006) 106-118
74. Sourjik V., and Berg H.C. Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci U S A 99 1 (2002) 123-127. This study is the first example to study the interaction of chemotaxis proteins in vivo using fluorescence resonance energy transfer (FRET).
75. Sourjik V., and Berg H.C. Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer. Proc Natl Acad Sci U S A 99 20 (2002) 12669-12674
76. Vaknin A., and Berg H.C. Single-cell FRET imaging of phosphatase activity in the Escherichia coli chemotaxis system. Proc Natl Acad Sci U S A 101 49 (2004) 17072-17077 PMCID: 535373
77. Kentner D., and Sourjik V. Dynamic map of protein interactions in the Escherichia coli chemotaxis pathway. Mol Syst Biol 5 (2009) 238 PMCID: 2644175
78. Sourjik V., Vaknin A., Shimizu T.S., and Berg H.C. In vivo measurement by FRET of pathway activity in bacterial chemotaxis. Methods Enzymol 423 (2007) 365-391
79. Gao R., Tao Y., and Stock A.M. System-level mapping of Escherichia coli response regulator dimerization with FRET hybrids. Mol Microbiol 69 6 (2008) 1358-1372 PMCID: 2586830
80. King S.T., and Kenney L.J. Application of fluorescence resonance energy transfer to examine EnvZ/OmpR interactions. Methods Enzymol 422 (2007) 352-360
81. Sciara M.I., Spagnuolo C., Jares-Erijman E., and Garcia Vescovi E. Cytolocalization of the PhoP response regulator in Salmonella enterica: modulation by extracellular Mg2+ and by the SCV environment. Mol Microbiol 70 2 (2008) 479-493
82. Galperin M.Y. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188 12 (2006) 4169-4182. PMCID: 1482966. A comprehensive domain analysis of bacterial response regulators.
83. Jenal U., and Galperin M.Y. Single domain response regulators: molecular switches with emerging roles in cell organization and dynamics. Curr Opin Microbiol 12 2 (2009) 152-160 PMCID: 2725762
84. Galperin M.Y. Diversity of structure and function of response regulator output domains. Curr Opin Microbiol (2010) 13
85. Barakat M., Ortet P., Jourlin-Castelli C., Ansaldi M., Mejean V., and Whitworth D.E. P2CS: a two-component system resource for prokaryotic signal transduction research. BMC Genomics 10 (2009) 315 PMCID: 2716373
86. White R.A., Szurmant H., Hoch J.A., and Hwa T. Features of protein-protein interactions in two-component signaling deduced from genomic libraries. Methods Enzymol 422 (2007) 75-101. A detailed analysis of protein interactions in TCS obtained from sequence data.
87. Szurmant H., Bobay B.G., White R.A., Sullivan D.M., Thompson R.J., Hwa T., et al. Co-evolving motions at protein-protein interfaces of two-component signaling systems identified by covariance analysis. Biochemistry 47 30 (2008) 7782-7784
88. Weigt M., White R.A., Szurmant H., Hoch J.A., and Hwa T. Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci U S A 106 1 (2009) 67-72. PMCID: 2629192
89. Szurmant H., Hoch, and James A. Interaction fidelity in two-component signaling. Curr Opin Microbiol (2010) 13
90. Skerker J.M., Perchuk B.S., Siryaporn A., Lubin E.A., Ashenberg O., Goulian M., et al. Rewiring the specificity of two-component signal transduction systems. Cell 133 6 (2008) 1043-1054 PMCID: 2453690