Molecular Mechanisms of Two-Component Signal Transduction

Journal of Molecular Biology

Volumn 428, Issue 19, 2016, Pages 3752-3775

  Zschiedrich, Christopher P ^a,b   Keidel, Victoria ^a,b   Szurmant, Hendrik ^a,b  

^a WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

response regulator; sensor histidine kinase; signal transduction; two component system

Indexed keywords

PROTEIN HISTIDINE KINASE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR;

AUTOPHOSPHORYLATION; BIOINFORMATICS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CYTOPLASM; DIMERIZATION; DNA BINDING; ENZYME ACTIVATION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA BINDING; SIGNAL DETECTION; SIGNAL TRANSDUCTION; STRUCTURAL MODEL; ARCHAEON; BACTERIUM; CHEMISTRY; ENZYMOLOGY; EUKARYOTE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ARCHAEA; BACTERIA; EUKARYOTA; GENE EXPRESSION REGULATION; HISTIDINE KINASE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84986601850     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.08.003     Document Type: Review

References (187)

1. [1] Ulrich, L.E., Zhulin, I.B., The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res. 38 (2010), D401–D407.
2. [2] Ortet, P., Whitworth, D.E., Santaella, C., Achouak, W., Barakat, M., P2CS: updates of the prokaryotic two-component systems database. Nucleic Acids Res. 43 (2015), D536–D541.
3. [3] Igo, M.M., Ninfa, A.J., Stock, J.B., Silhavy, T.J., Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev. 3 (1989), 1725–1734.
4. [4] Szurmant, H., White, R.A., Hoch, J.A., Sensor complexes regulating two-component signal transduction. Curr. Opin. Struct. Biol. 17 (2007), 706–715.
5. [5] Szurmant, H., Hoch, J.A., Interaction fidelity in two-component signaling. Curr. Opin. Microbiol. 13 (2010), 190–197.
6. [6] Gao, R., Stock, A.M., Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr. Opin. Microbiol. 13 (2010), 160–167.
7. [7] Mascher, T., Helmann, J.D., Unden, G., Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70 (2006), 910–938.
8. [8] Bhate, M.P., Molnar, K.S., Goulian, M., DeGrado, W.F., Signal transduction in histidine kinases: insights from new structures. Structure 23 (2015), 981–994.
9. [9] Albanesi, D., Martin, M., Trajtenberg, F., Mansilla, M.C., Haouz, A., Alzari, P.M., de Mendoza, D., Buschiazzo, A., Structural plasticity and catalysis regulation of a thermosensor histidine kinase. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 16,185–16,190.
10. [10] Moglich, A., Ayers, R.A., Moffat, K., Design and signaling mechanism of light-regulated histidine kinases. J. Mol. Biol. 385 (2009), 1433–1444.
11. [11] Diensthuber, R.P., Bommer, M., Gleichmann, T., Moglich, A., Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators. Structure 21 (2013), 1127–1136.
12. [12] Wagner, J.R., Brunzelle, J.S., Forest, K.T., Vierstra, R.D., A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438 (2005), 325–331.
13. [13] Karniol, B., Wagner, J.R., Walker, J.M., Vierstra, R.D., Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem. J. 392 (2005), 103–116.
14. [14] Sevvana, M., Vijayan, V., Zweckstetter, M., Reinelt, S., Madden, D.R., Herbst-Irmer, R., Sheldrick, G.M., Bott, M., Griesinger, C., Becker, S., A ligand-induced switch in the periplasmic domain of sensor histidine kinase CitA. J. Mol. Biol. 377 (2008), 512–523.
15. [15] Wu, R., Gu, M., Wilton, R., Babnigg, G., Kim, Y., Pokkuluri, P.R., Szurmant, H., Joachimiak, A., Schiffer, M., Insight into the sporulation phosphorelay: crystal structure of the sensor domain of Bacillus subtilis histidine kinase, KinD. Protein Sci. 22 (2013), 564–576.
16. [16] Cheung, J., Hendrickson, W.A., Structural analysis of ligand stimulation of the histidine kinase NarX. Structure 17 (2009), 190–201.
17. [17] Bader, M.W., Sanowar, S., Daley, M.E., Schneider, A.R., Cho, U., Xu, W., Klevit, R.E., Le Moual, H., Miller, S.I., Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122 (2005), 461–472.
18. [18] Unden, G., Nilkens, S., Singenstreu, M., Bacterial sensor kinases using Fe–S cluster binding PAS or GAF domains for O2 sensing. Dalton Trans. 42 (2013), 3082–3087.
19. [19] Neiditch, M.B., Federle, M.J., Pompeani, A.J., Kelly, R.C., Swem, D.L., Jeffrey, P.D., Bassler, B.L., Hughson, F.M., Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126 (2006), 1095–1108.
20. [20] Szurmant, H., Mohan, M.A., Imus, P.M., Hoch, J.A., YycH and YycI interact to regulate the essential YycFG two-component system in Bacillus subtilis. J. Bacteriol. 189 (2007), 3280–3289.
21. [21] Mascher, T., Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria. FEMS Microbiol. Lett. 264 (2006), 133–144.
22. [22] Moglich, A., Ayers, R.A., Moffat, K., Structure and signaling mechanism of Per-ARNT-Sim domains. Structure. 17 (2009), 1282–1294.
23. [23] Zhang, Z., Hendrickson, W.A., Structural characterization of the predominant family of histidine kinase sensor domains. J. Mol. Biol. 400 (2010), 335–353.
24. [24] Ponting, C.P., Aravind, L., PAS: a multifunctional domain family comes to light. Curr. Biol. 7 (1997), R674–R677.
25. [25] Shah, N., Gaupp, R., Moriyama, H., Eskridge, K.M., Moriyama, E.N., Somerville, G.A., Reductive evolution and the loss of PDC/PAS domains from the genus Staphylococcus. BMC Genomics, 14, 2013, 524.
26. [26] Reinelt, S., Hofmann, E., Gerharz, T., Bott, M., Madden, D.R., The structure of the periplasmic ligand-binding domain of the sensor kinase CitA reveals the first extracellular PAS domain. J. Biol. Chem. 278 (2003), 39,189–39,196.
27. [27] Pappalardo, L., Janausch, I.G., Vijayan, V., Zientz, E., Junker, J., Peti, W., Zweckstetter, M., Unden, G., Griesinger, C., The NMR structure of the sensory domain of the membranous two-component fumarate sensor (histidine protein kinase) DcuS of Escherichia coli. J. Biol. Chem. 278 (2003), 39,185–39,188.
28. [28] Chang, C., Tesar, C., Gu, M., Babnigg, G., Joachimiak, A., Pokkuluri, P.R., Szurmant, H., Schiffer, M., Extracytoplasmic PAS-like domains are common in signal transduction proteins. J. Bacteriol. 192 (2010), 1156–1159.
29. [29] Shi, L., Hulett, F.M., The cytoplasmic kinase domain of PhoR is sufficient for the low phosphate-inducible expression of pho regulon genes in Bacillus subtilis. Mol. Microbiol. 31 (1999), 211–222.
30. [30] Botella, E., Devine, S.K., Hubner, S., Salzberg, L.I., Gale, R.T., Brown, E.D., Link, H., Sauer, U., Codee, J.D., Noone, D., Devine, K.M., PhoR autokinase activity is controlled by an intermediate in wall teichoic acid metabolism that is sensed by the intracellular PAS domain during the PhoPR-mediated phosphate limitation response of Bacillus subtilis. Mol. Microbiol. 94 (2014), 1242–1259.
31. [31] Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B.L., Hughson, F.M., Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415 (2002), 545–549.
32. [32] Milburn, M.V., Prive, G.G., Milligan, D.L., Scott, W.G., Yeh, J., Jancarik, J., Koshland, D.E. Jr., Kim, S.H., Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science. 254 (1991), 1342–1347.
33. [33] Winkler, K., Schultz, A., Schultz, J.E., The S-helix determines the signal in a Tsr receptor/adenylyl cyclase reporter. J. Biol. Chem. 287 (2012), 15,479–15,488.
34. [34] Moore, J.O., Hendrickson, W.A., An asymmetry-to-symmetry switch in signal transmission by the histidine kinase receptor for TMAO. Structure 20 (2012), 729–741.
35. [35] Shu, C.J., Ulrich, L.E., Zhulin, I.B., The NIT domain: a predicted nitrate-responsive module in bacterial sensory receptors. Trends Biochem. Sci. 28 (2003), 121–124.
36. [36] Chervitz, S.A., Falke, J.J., Molecular mechanism of transmembrane signaling by the aspartate receptor: a model. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 2545–2550.
37. [37] Falke, J.J., Erbse, A.H., The piston rises again. Structure. 17 (2009), 1149–1151.
38. [38] Molnar, K.S., Bonomi, M., Pellarin, R., Clinthorne, G.D., Gonzalez, G., Goldberg, S.D., Goulian, M., Sali, A., DeGrado, W.F., Cys-scanning disulfide crosslinking and bayesian modeling probe the transmembrane signaling mechanism of the histidine kinase, PhoQ. Structure. 22 (2014), 1239–1251.
39. [39] Lowe, E.C., Basle, A., Czjzek, M., Firbank, S.J., Bolam, D.N., A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 7298–7303.
40. [40] Glekas, G.D., Foster, R.M., Cates, J.R., Estrella, J.A., Wawrzyniak, M.J., Rao, C.V., Ordal, G.W., A PAS domain binds asparagine in the chemotaxis receptor McpB in Bacillus subtilis. J. Biol. Chem. 285 (2010), 1870–1878.
41. [41] Szurmant, H., Bunn, M.W., Cho, S.H., Ordal, G.W., Ligand-induced conformational changes in the Bacillus subtilis chemoreceptor McpB determined by disulfide crosslinking in vivo. J. Mol. Biol. 344 (2004), 919–928.
42. [42] Zhou, Y.F., Nan, B., Nan, J., Ma, Q., Panjikar, S., Liang, Y.H., Wang, Y., Su, X.D., C4-dicarboxylates sensing mechanism revealed by the crystal structures of DctB sensor domain. J. Mol. Biol. 383 (2008), 49–61.
43. [43] Aguilar, P.S., Hernandez-Arriaga, A.M., Cybulski, L.E., Erazo, A.C., de Mendoza, D., Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J. 20 (2001), 1681–1691.
44. [44] Jiang, M., Shao, W., Perego, M., Hoch, J.A., Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38 (2000), 535–542.
45. [45] Maslennikov, I., Klammt, C., Hwang, E., Kefala, G., Okamura, M., Esquivies, L., Mors, K., Glaubitz, C., Kwiatkowski, W., Jeon, Y.H., Choe, S., Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 10,902–10,907.
46. [46] Goldberg, S.D., Clinthorne, G.D., Goulian, M., DeGrado, W.F., Transmembrane polar interactions are required for signaling in the Escherichia coli sensor kinase PhoQ. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 8141–8146.
47. [47] Lemmin, T., Soto, C.S., Clinthorne, G., DeGrado, W.F., Dal Peraro, M., Assembly of the transmembrane domain of E. coli PhoQ histidine kinase: implications for signal transduction from molecular simulations. PLoS Comput. Biol., 9, 2013, e1002878.
48. [48] Szurmant, H., Bu, L., Brooks, C.L. III, Hoch, J.A., An essential sensor histidine kinase controlled by transmembrane helix interactions with its auxiliary proteins. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 5891–5896.
49. [49] Saita, E., Albanesi, D., de Mendoza, D., Sensing membrane thickness: lessons learned from cold stress. Biochim. Biophys. Acta., 2016, 837–846.
50. [50] Cybulski, L.E., Martin, M., Mansilla, M.C., Fernandez, A., de Mendoza, D., Membrane thickness cue for cold sensing in a bacterium. Curr. Biol. 20 (2010), 1539–1544.
51. [51] Aravind, L., Ponting, C.P., The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol. Lett. 176 (1999), 111–116.
52. [52] Ferris, H.U., Dunin-Horkawicz, S., Mondejar, L.G., Hulko, M., Hantke, K., Martin, J., Schultz, J.E., Zeth, K., Lupas, A.N., Coles, M., The mechanisms of HAMP-mediated signaling in transmembrane receptors. Structure 19 (2011), 378–385.
53. [53] Hulko, M., Berndt, F., Gruber, M., Linder, J.U., Truffault, V., Schultz, A., Martin, J., Schultz, J.E., Lupas, A.N., Coles, M., The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126 (2006), 929–940.
54. [54] Airola, M.V., Watts, K.J., Bilwes, A.M., Crane, B.R., Structure of concatenated HAMP domains provides a mechanism for signal transduction. Structure. 18 (2010), 436–448.
55. [55] Swain, K.E., Falke, J.J., Structure of the conserved HAMP domain in an intact, membrane-bound chemoreceptor: a disulfide mapping study. Biochemistry. 46 (2007), 13,684–13,695.
56. [56] Swain, K.E., Gonzalez, M.A., Falke, J.J., Engineered socket study of signaling through a four-helix bundle: evidence for a yin-yang mechanism in the kinase control module of the aspartate receptor. Biochemistry 48 (2009), 9266–9277.
57. [57] Parkinson, J.S., Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases. Annu. Rev. Microbiol. 64 (2010), 101–122.
58. [58] Stewart, V., The HAMP signal-conversion domain: static two-state or dynamic three-state?. Mol. Microbiol. 91 (2014), 853–857.
59. [59] Tews, I., Findeisen, F., Sinning, I., Schultz, A., Schultz, J.E., Linder, J.U., The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science. 308 (2005), 1020–1023.
60. [60] Mechaly, A.E., Sassoon, N., Betton, J.M., Alzari, P.M., Segmental helical motions and dynamical asymmetry modulate histidine kinase autophosphorylation. PLoS Biol., 12, 2014, e1001776.
61. [61] Korycinski, M., Albrecht, R., Ursinus, A., Hartmann, M.D., Coles, M., Martin, J., Dunin-Horkawicz, S., Lupas, A.N., STAC–a new domain associated with transmembrane solute transport and two-component signal transduction systems. J. Mol. Biol. 427 (2015), 3327–3339.
62. [62] Zhang, X.X., Rainey, P.B., Dual involvement of CbrAB and NtrBC in the regulation of histidine utilization in Pseudomonas fluorescens SBW25. Genetics 178 (2008), 185–195.
63. [63] Taylor, B.L., Zhulin, I.B., PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63 (1999), 479–506.
64. [64] Mullner, M., Hammel, O., Mienert, B., Schlag, S., Bill, E., Unden, G., A PAS domain with an oxygen labile [4Fe–4S](2 +) cluster in the oxygen sensor kinase NreB of Staphylococcus carnosus. Biochemistry 47 (2008), 13,921–13,932.
65. [65] Kamps, A., Achebach, S., Fedtke, I., Unden, G., Gotz, F., Staphylococcal NreB: an O(2)-sensing histidine protein kinase with an O(2)-labile iron–sulphur cluster of the FNR type. Mol. Microbiol. 52 (2004), 713–723.
66. [66] Key, J., Srajer, V., Pahl, R., Moffat, K., Time-resolved crystallographic studies of the heme domain of the oxygen sensor FixL: structural dynamics of ligand rebinding and their relation to signal transduction. Biochemistry. 46 (2007), 4706–4715.
67. [67] Gong, W., Hao, B., Mansy, S.S., Gonzalez, G., Gilles-Gonzalez, M.A., Chan, M.K., Structure of a biological oxygen sensor: a new mechanism for heme-driven signal transduction. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 15,177–15,182.
68. [68] Gong, W., Hao, B., Chan, M.K., New mechanistic insights from structural studies of the oxygen-sensing domain of Bradyrhizobium japonicum FixL. Biochemistry. 39 (2000), 3955–3962.
69. [69] Hao, B., Isaza, C., Arndt, J., Soltis, M., Chan, M.K., Structure-based mechanism of O2 sensing and ligand discrimination by the FixL heme domain of Bradyrhizobium japonicum. Biochemistry. 41 (2002), 12,952–12,958.
70. [70] Ward, S.M., Delgado, A., Gunsalus, R.P., Manson, M.D., A NarX-Tar chimera mediates repellent chemotaxis to nitrate and nitrite. Mol. Microbiol. 44 (2002), 709–719.
71. [71] Jin, T., Inouye, M., Ligand binding to the receptor domain regulates the ratio of kinase to phosphatase activities of the signaling domain of the hybrid Escherichia coli transmembrane receptor, Taz1. J. Mol. Biol. 232 (1993), 484–492.
72. [72] Wang, C., Sang, J., Wang, J., Su, M., Downey, J.S., Wu, Q., Wang, S., Cai, Y., Xu, X., Wu, J., Senadheera, D.B., Cvitkovitch, D.G., Chen, L., Goodman, S.D., Han, A., Mechanistic insights revealed by the crystal structure of a histidine kinase with signal transducer and sensor domains. PLoS Biol., 11, 2013, e1001493.
73. [73] Ferris, H.U., Dunin-Horkawicz, S., Hornig, N., Hulko, M., Martin, J., Schultz, J.E., Zeth, K., Lupas, A.N., Coles, M., Mechanism of regulation of receptor histidine kinases. Structure 20 (2012), 56–66.
74. [74] Saita, E., Abriata, L.A., Tsai, Y.T., Trajtenberg, F., Lemmin, T., Buschiazzo, A., Dal Peraro, M., de Mendoza, D., Albanesi, D., A coiled coil switch mediates cold sensing by the thermosensory protein DesK. Mol. Microbiol. 98 (2015), 258–271.
75. [75] Rivera-Cancel, G., Ko, W.H., Tomchick, D.R., Correa, F., Gardner, K.H., Full-length structure of a monomeric histidine kinase reveals basis for sensory regulation. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 17,839–17,844.
76. [76] Dago, A.E., Schug, A., Procaccini, A., Hoch, J.A., Weigt, M., Szurmant, H., Structural basis of histidine kinase autophosphorylation deduced by integrating genomics, molecular dynamics, and mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E1733–E1742.
77. [77] Trajtenberg, F., Grana, M., Ruetalo, N., Botti, H., Buschiazzo, A., Structural and enzymatic insights into the ATP binding and autophosphorylation mechanism of a sensor histidine kinase. J. Biol. Chem. 285 (2010), 24,892–24,903.
78. [78] Weigt, M., White, R.A., Szurmant, H., Hoch, J.A., Hwa, T., Identification of direct residue contacts in protein–protein interaction by message passing. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 67–72.
79. [79] Ninfa, E.G., Atkinson, M.R., Kamberov, E.S., Ninfa, A.J., Mechanism of autophosphorylation of Escherichia coli nitrogen regulator II (NRII or NtrB): trans-phosphorylation between subunits. J. Bacteriol. 175 (1993), 7024–7032.
80. [80] Swanson, R.V., Bourret, R.B., Simon, M.I., Intermolecular complementation of the kinase activity of CheA. Mol. Microbiol. 8 (1993), 435–441.
81. [81] Casino, P., Rubio, V., Marina, A., Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell. 139 (2009), 325–336.
82. [82] Pena-Sandoval, G.R., Georgellis, D., The ArcB sensor kinase of Escherichia coli autophosphorylates by an intramolecular reaction. J. Bacteriol. 192 (2010), 1735–1739.
83. [83] Marina, A., Waldburger, C.D., Hendrickson, W.A., Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J. 24 (2005), 4247–4259.
84. [84] Ashenberg, O., Keating, A.E., Laub, M.T., Helix bundle loops determine whether histidine kinases autophosphorylate in cis or in trans. J. Mol. Biol. 425 (2013), 1198–1209.
85. [85] Casino, P., Miguel-Romero, L., Marina, A., Visualizing autophosphorylation in histidine kinases. Nat. Commun., 5, 2014, 3258.
86. [86] Jiang, P., Peliska, J.A., Ninfa, A.J., Asymmetry in the autophosphorylation of the two-component regulatory system transmitter protein nitrogen regulator II of Escherichia coli. Biochemistry 39 (2000), 5057–5065.
87. [87] Laub, M.T., Goulian, M., Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41 (2007), 121–145.
88. [88] Yamamoto, K., Hirao, K., Oshima, T., Aiba, H., Utsumi, R., Ishihama, A., Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280 (2005), 1448–1456.
89. [89] Skerker, J.M., Prasol, M.S., Perchuk, B.S., Biondi, E.G., Laub, M.T., Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol., 3, 2005, e334.
90. [90] Siryaporn, A., Goulian, M., Characterizing cross-talk in vivo avoiding pitfalls and overinterpretation. Methods Enzymol. 471 (2010), 1–16.
91. [91] Wolfe, A.J., Physiologically relevant small phosphodonors link metabolism to signal transduction. Curr. Opin. Microbiol. 13 (2010), 204–209.
92. [92] Tzeng, Y.L., Hoch, J.A., Molecular recognition in signal transduction: the interaction surfaces of the Spo0F response regulator with its cognate phosphorelay proteins revealed by alanine scanning mutagenesis. J. Mol. Biol. 272 (1997), 200–212.
93. [93] Zapf, J., Sen, U., Madhusudan, Hoch, J.A., Varughese, K.I., 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 (2000), 851–862.
94. [94] Stephenson, K., Hoch, J.A., Evolution of signalling in the sporulation phosphorelay. Mol. Microbiol. 46 (2002), 297–304.
95. [95] K.I. Varughese, Madhusudan, X.Z. Zhou, J.M. Whiteley, J.A. Hoch, Formation of a novel four-helix bundle and molecular recognition sites by dimerization of a response regulator phosphotransferase, Mol. Cell. 2 (1998) 485–493.
96. [96] Hoch, J.A., Varughese, K.I., Keeping signals straight in phosphorelay signal transduction. J. Bacteriol. 183 (2001), 4941–4949.
97. [97] Li, L., Shakhnovich, E.I., Mirny, L.A., Amino acids determining enzyme-substrate specificity in prokaryotic and eukaryotic protein kinases. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 4463–4468.
98. [98] White, R.A., Szurmant, H., Hoch, J.A., Hwa, T., Features of protein–protein interactions in two-component signaling deduced from genomic libraries. Methods Enzymol. 422 (2007), 75–101.
99. [99] Burger, L., van Nimwegen, E., Accurate prediction of protein–protein interactions from sequence alignments using a Bayesian method. Mol. Syst. Biol., 4, 2008, 165.
100. [100] Szurmant, H., Bobay, B.G., White, R.A., Sullivan, D.M., Thompson, R.J., Hwa, T., Hoch, J.A., Cavanagh, J., Co-evolving motions at protein–protein interfaces of two-component signaling systems identified by covariance analysis. Biochemistry 47 (2008), 7782–7784.
101. [101] Skerker, J.M., Perchuk, B.S., Siryaporn, A., Lubin, E.A., Ashenberg, O., Goulian, M., Laub, M.T., Rewiring the specificity of two-component signal transduction systems. Cell. 133 (2008), 1043–1054.
102. [102] Siryaporn, A., Perchuk, B.S., Laub, M.T., Goulian, M., Evolving a robust signal transduction pathway from weak cross-talk. Mol. Syst. Biol., 6, 2010, 452.
103. [103] Lunt, B., Szurmant, H., Procaccini, A., Hoch, J.A., Hwa, T., Weigt, M., Inference of direct residue contacts in two-component signaling. Methods Enzymol. 471 (2010), 17–41.
104. [104] Schug, A., Weigt, M., Onuchic, J.N., Hwa, T., Szurmant, H., High-resolution protein complexes from integrating genomic information with molecular simulation. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 22,124–22,129.
105. [105] Schug, A., Weigt, M., Hoch, J.A., Onuchic, J.N., Hwa, T., Szurmant, H., Computational modeling of phosphotransfer complexes in two-component signaling. Methods Enzymol. 471 (2010), 43–58.
106. [106] Szurmant, H., Hoch, J.A., Statistical analyses of protein sequence alignments identify structures and mechanisms in signal activation of sensor histidine kinases. Mol. Microbiol. 87 (2013), 707–712.
107. [107] Feinauer, C., Szurmant, H., Weigt, M., Pagnani, A., Inter-protein sequence co-evolution predicts known physical interactions in bacterial ribosomes and the Trp operon. PLoS One, 11, 2016, e0149166.
108. [108] Sulkowska, J.I., Morcos, F., Weigt, M., Hwa, T., Onuchic, J.N., Genomics-aided structure prediction. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 10,340–10,345.
109. [109] Ovchinnikov, S., Kamisetty, H., Baker, D., Robust and accurate prediction of residue-residue interactions across protein interfaces using evolutionary information. Elife, 3, 2014, e02030.
110. [110] Ovchinnikov, S., Kinch, L., Park, H., Liao, Y., Pei, J., Kim, D.E., Kamisetty, H., Grishin, N.V., Baker, D., Large-scale determination of previously unsolved protein structures using evolutionary information. Elife, 4, 2015, e09248.
111. [111] Procaccini, A., Lunt, B., Szurmant, H., Hwa, T., Weigt, M., Dissecting the specificity of protein–protein interaction in bacterial two-component signaling: orphans and crosstalks. PLoS One, 6, 2011, e19729.
112. [112] Dworkin, J., Ser/Thr phosphorylation as a regulatory mechanism in bacteria. Curr. Opin. Microbiol. 24 (2015), 47–52.
113. [113] Wright, D.P., Ulijasz, A.T., Regulation of transcription by eukaryotic-like serine-threonine kinases and phosphatases in Gram-positive bacterial pathogens. Virulence 5 (2014), 863–885.
114. [114] Fridman, M., Williams, G.D., Muzamal, U., Hunter, H., Siu, K.W., Golemi-Kotra, D., Two unique phosphorylation-driven signaling pathways crosstalk in Staphylococcus aureus to modulate the cell-wall charge: Stk1/Stp1 meets GraSR. Biochemistry 52 (2013), 7975–7986.
115. [115] Canova, M.J., Baronian, G., Brelle, S., Cohen-Gonsaud, M., Bischoff, M., Molle, V., A novel mode of regulation of the Staphylococcus aureus vancomycin-resistance-associated response regulator VraR mediated by Stk1 protein phosphorylation. Biochem. Biophys. Res. Commun. 447 (2014), 165–171.
116. [116] Chao, J.D., Papavinasasundaram, K.G., Zheng, X., Chavez-Steenbock, A., Wang, X., Lee, G.Q., Av-Gay, Y., Convergence of Ser/Thr and two-component signaling to coordinate expression of the dormancy regulon in mycobacterium tuberculosis. J. Biol. Chem. 285 (2010), 29,239–29,246.
117. [117] Canova, M.J., Veyron-Churlet, R., Zanella-Cleon, I., Cohen-Gonsaud, M., Cozzone, A.J., Becchi, M., Kremer, L., Molle, V., The Mycobacterium tuberculosis serine/threonine kinase PknL phosphorylates Rv2175c: mass spectrometric profiling of the activation loop phosphorylation sites and their role in the recruitment of Rv2175c. Proteomics 8 (2008), 521–533.
118. [118] Cohen-Gonsaud, M., Barthe, P., Canova, M.J., Stagier-Simon, C., Kremer, L., Roumestand, C., Molle, V., The Mycobacterium tuberculosis Ser/Thr kinase substrate Rv2175c is a DNA-binding protein regulated by phosphorylation. J. Biol. Chem. 284 (2009), 19,290–19,300.
119. [119] Ulijasz, A.T., Falk, S.P., Weisblum, B., Phosphorylation of the RitR DNA-binding domain by a Ser-Thr phosphokinase: implications for global gene regulation in the streptococci. Mol. Microbiol. 71 (2009), 382–390.
120. [120] Agarwal, S., Agarwal, S., Pancholi, P., Pancholi, V., Strain-specific regulatory role of eukaryote-like serine/threonine phosphatase in pneumococcal adherence. Infect. Immun. 80 (2012), 1361–1372.
121. [121] Lin, W.J., Walthers, D., Connelly, J.E., Burnside, K., Jewell, K.A., Kenney, L.J., Rajagopal, L., Threonine phosphorylation prevents promoter DNA binding of the group B Streptococcus response regulator CovR. Mol. Microbiol. 71 (2009), 1477–1495.
122. [122] Horstmann, N., Saldana, M., Sahasrabhojane, P., Yao, H., Su, X., Thompson, E., Koller, A., Shelburne, S.A. III, Dual-site phosphorylation of the control of virulence regulator impacts group a streptococcal global gene expression and pathogenesis. PLoS Pathog., 10, 2014, e1004088.
123. [123] Libby, E.A., Goss, L.A., Dworkin, J., The eukaryotic-like Ser/Thr kinase PrkC regulates the essential WalRK two-component system in Bacillus subtilis. PLoS Genet., 11, 2015, e1005275.
124. [124] Gao, R., Stock, A.M., Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63 (2009), 133–154.
125. [125] Szurmant, H., Ordal, G.W., Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol. Mol. Biol. Rev. 68 (2004), 301–319.
126. [126] Wang, L., Tian, X., Wang, J., Yang, H., Fan, K., Xu, G., Yang, K., Tan, H., Autoregulation of antibiotic biosynthesis by binding of the end product to an atypical response regulator. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 8617–8622.
127. [127] Madhusudan, M., Zapf, J., Hoch, J.A., Whiteley, J.M., Xuong, N.H., Varughese, K.I., A response regulatory protein with the site of phosphorylation blocked by an arginine interaction: crystal structure of Spo0F from Bacillus subtilis. Biochemistry 36 (1997), 12,739–12,745.
128. [128] Baikalov, I., Schroder, I., Kaczor-Grzeskowiak, M., Grzeskowiak, K., Gunsalus, R.P., Dickerson, R.E., Structure of the Escherichia coli response regulator NarL. Biochemistry 35 (1996), 11,053–11,061.
129. [129] Sola, M., Gomis-Ruth, F.X., Serrano, L., Gonzalez, A., Coll, M., Three-dimensional crystal structure of the transcription factor PhoB receiver domain. J. Mol. Biol. 285 (1999), 675–687.
130. [130] Stock, A.M., Robinson, V.L., Goudreau, P.N., Two-component signal transduction. Annu. Rev. Biochem. 69 (2000), 183–215.
131. [131] Bourret, R.B., Receiver domain structure and function in response regulator proteins. Curr. Opin. Microbiol. 13 (2010), 142–149.
132. [132] Hong, E., Lee, H.M., Ko, H., Kim, D.U., Jeon, B.Y., Jung, J., Shin, J., Lee, S.A., Kim, Y., Jeon, Y.H., Cheong, C., Cho, H.S., Lee, W., Structure of an atypical orphan response regulator protein supports a new phosphorylation-independent regulatory mechanism. J. Biol. Chem. 282 (2007), 20,667–20,675.
133. [133] Im, Y.J., Rho, S.H., Park, C.M., Yang, S.S., Kang, J.G., Lee, J.Y., Song, P.S., Eom, S.H., Crystal structure of a cyanobacterial phytochrome response regulator. Protein Sci. 11 (2002), 614–624.
134. [134] Benda, C., Scheufler, C., Tandeau de Marsac, N., Gartner, W., Crystal structures of two cyanobacterial response regulators in apo- and phosphorylated form reveal a novel dimerization motif of phytochrome-associated response regulators. Biophys. J. 87 (2004), 476–487.
135. [135] Davies, K.M., Lowe, E.D., Venien-Bryan, C., Johnson, L.N., The HupR receiver domain crystal structure in its nonphospho and inhibitory phospho states. J. Mol. Biol. 385 (2009), 51–64.
136. [136] Birck, C., Mourey, L., Gouet, P., Fabry, B., Schumacher, J., Rousseau, P., Kahn, D., Samama, J.P., Conformational changes induced by phosphorylation of the FixJ receiver domain. Structure 7 (1999), 1505–1515.
137. [137] Fernandez, I., Otero, L.H., Klinke, S., Carrica Mdel, C., Goldbaum, F.A., Snapshots of conformational changes shed light into the NtrX receiver domain signal transduction mechanism. J. Mol. Biol. 427 (2015), 3258–3272.
138. [138] Park, A.K., Moon, J.H., Lee, K.S., Chi, Y.M., Crystal structure of receiver domain of putative NarL family response regulator spr1814 from Streptococcus pneumoniae in the absence and presence of the phosphoryl analog beryllofluoride. Biochem. Biophys. Res. Commun. 421 (2012), 403–407.
139. [139] Leonard, P.G., Golemi-Kotra, D., Stock, A.M., Phosphorylation-dependent conformational changes and domain rearrangements in Staphylococcus aureus VraR activation. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 8525–8530.
140. [140] Trajtenberg, F., Albanesi, D., Ruetalo, N., Botti, H., Mechaly, A.E., Nieves, M., Aguilar, P.S., Cybulski, L., Larrieux, N., de Mendoza, D., Buschiazzo, A., Allosteric activation of bacterial response regulators: the role of the cognate histidine kinase beyond phosphorylation. MBio., 5, 2014, e02105.
141. [141] Park, A.K., Moon, J.H., Oh, J.S., Lee, K.S., Chi, Y.M., Crystal structure of the response regulator spr1814 from Streptococcus pneumoniae reveals unique interdomain contacts among NarL family proteins. Biochem. Biophys. Res. Commun. 434 (2013), 65–69.
142. [142] Lee, S.Y., De La Torre, A., Yan, D., Kustu, S., Nixon, B.T., Wemmer, D.E., Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA + ATPase domains. Genes Dev. 17 (2003), 2552–2563.
143. [143] Lee, S.Y., Cho, H.S., Pelton, J.G., Yan, D., Henderson, R.K., King, D.S., Huang, L., Kustu, S., Berry, E.A., Wemmer, D.E., Crystal structure of an activated response regulator bound to its target. Nat. Struct. Biol. 8 (2001), 52–56.
144. [144] Villali, J., Pontiggia, F., Clarkson, M.W., Hagan, M.F., Kern, D., Evidence against the “Y-T coupling” mechanism of activation in the response regulator NtrC. J. Mol. Biol. 426 (2014), 1554–1567.
145. [145] Schuster, M., Silversmith, R.E., Bourret, R.B., Conformational coupling in the chemotaxis response regulator CheY. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 6003–6008.
146. [146] Volkman, B.F., Lipson, D., Wemmer, D.E., Kern, D., Two-state allosteric behavior in a single-domain signaling protein. Science. 291 (2001), 2429–2433.
147. [147] Feher, V.A., Cavanagh, J., Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F. Nature. 400 (1999), 289–293.
148. [148] Ocasio, V.J., Correa, F., Gardner, K.H., Ligand-induced folding of a two-component signaling receiver domain. Biochemistry 54 (2015), 1353–1363.
149. [149] Thomas, S.A., Brewster, J.A., Bourret, R.B., Two variable active site residues modulate response regulator phosphoryl group stability. Mol. Microbiol. 69 (2008), 453–465.
150. [150] Pazy, Y., Wollish, A.C., Thomas, S.A., Miller, P.J., Collins, E.J., Bourret, R.B., Silversmith, R.E., Matching biochemical reaction kinetics to the timescales of life: structural determinants that influence the autodephosphorylation rate of response regulator proteins. J. Mol. Biol. 392 (2009), 1205–1220.
151. [151] Silversmith, R.E., Auxiliary phosphatases in two-component signal transduction. Curr. Opin. Microbiol. 13 (2010), 177–183.
152. [152] Silversmith, R.E., Levin, M.D., Schilling, E., Bourret, R.B., Kinetic characterization of catalysis by the chemotaxis phosphatase CheZ. Modulation of activity by the phosphorylated CheY substrate. J. Biol. Chem. 283 (2008), 756–765.
153. [153] Pazy, Y., Motaleb, M.A., Guarnieri, M.T., Charon, N.W., Zhao, R., Silversmith, R.E., Identical phosphatase mechanisms achieved through distinct modes of binding phosphoprotein substrate. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 1924–1929.
154. [154] Kirby, J.R., Kristich, C.J., Saulmon, M.M., Zimmer, M.A., Garrity, L.F., Zhulin, I.B., Ordal, G.W., CheC is related to the family of flagellar switch proteins and acts independently from CheD to control chemotaxis in Bacillus subtilis. Mol. Microbiol. 42 (2001), 573–585.
155. [155] Zhao, R., Collins, E.J., Bourret, R.B., Silversmith, R.E., Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat. Struct. Biol. 9 (2002), 570–575.
156. [156] Perego, M., Hanstein, C., Welsh, K.M., Djavakhishvili, T., Glaser, P., Hoch, J.A., Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell 79 (1994), 1047–1055.
157. [157] Ohlsen, K.L., Grimsley, J.K., Hoch, J.A., Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 1756–1760.
158. [158] Parashar, V., Mirouze, N., Dubnau, D.A., Neiditch, M.B., Structural basis of response regulator dephosphorylation by rap phosphatases. PLoS Biol., 9, 2011, e1000589.
159. [159] Park, S.Y., Chao, X., Gonzalez-Bonet, G., Beel, B.D., Bilwes, A.M., Crane, B.R., Structure and function of an unusual family of protein phosphatases: the bacterial chemotaxis proteins CheC and CheX. Mol. Cell. 16 (2004), 563–574.
160. [160] Grenha, R., Rzechorzek, N.J., Brannigan, J.A., de Jong, R.N., Ab, E., Diercks, T., Truffault, V., Ladds, J.C., Fogg, M.J., Bongiorni, C., Perego, M., Kaptein, R., Wilson, K.S., Folkers, G.E., Wilkinson, A.J., Structural characterization of Spo0E-like protein-aspartic acid phosphatases that regulate sporulation in bacilli. J. Biol. Chem. 281 (2006), 37,993–38,003.
161. [161] Diaz, A.R., Stephenson, S., Green, J.M., Levdikov, V.M., Wilkinson, A.J., Perego, M., Functional role for a conserved aspartate in the Spo0E signature motif involved in the dephosphorylation of the Bacillus subtilis sporulation regulator Spo0A. J. Biol. Chem. 283 (2008), 2962–2972.
162. [162] Martinez-Hackert, E., Stock, A.M., Structural relationships in the OmpR family of winged-helix transcription factors. J. Mol. Biol. 269 (1997), 301–312.
163. [163] Nikolskaya, A.N., Galperin, M.Y., A novel type of conserved DNA-binding domain in the transcriptional regulators of the AlgR/AgrA/LytR family. Nucleic Acids Res. 30 (2002), 2453–2459.
164. [164] Nguyen, M.P., Yoon, J.M., Cho, M.H., Lee, S.W., Prokaryotic 2-component systems and the OmpR/PhoB superfamily. Can. J. Microbiol. 61 (2015), 799–810.
165. [165] Vashist, A., Prithvi Raj, D., Gupta, U.D., Bhat, R., Tyagi, J.S., The alpha10 helix of DevR, the Mycobacterium tuberculosis dormancy response regulator, regulates its DNA binding and activity. FEBS J. 283 (2016), 1286–1299.
166. [166] Batchelor, J.D., Sterling, H.J., Hong, E., Williams, E.R., Wemmer, D.E., Receiver domains control the active-state stoichiometry of Aquifex aeolicus sigma54 activator NtrC4, as revealed by electrospray ionization mass spectrometry. J. Mol. Biol. 393 (2009), 634–643.
167. [167] Sidote, D.J., Barbieri, C.M., Wu, T., Stock, A.M., Structure of the Staphylococcus aureus AgrA LytTR domain bound to DNA reveals a beta fold with an unusual mode of binding. Structure 16 (2008), 727–735.
168. [168] Boudes, M., Sanchez, D., Graille, M., van Tilbeurgh, H., Durand, D., Quevillon-Cheruel, S., Structural insights into the dimerization of the response regulator ComE from Streptococcus pneumoniae. Nucleic Acids Res. 42 (2014), 5302–5313.
169. [169] O'Hara, B.P., Norman, R.A., Wan, P.T., Roe, S.M., Barrett, T.E., Drew, R.E., Pearl, L.H., Crystal structure and induction mechanism of AmiC-AmiR: a ligand-regulated transcription antitermination complex. EMBO J. 18 (1999), 5175–5186.
170. [170] Shu, C.J., Zhulin, I.B., ANTAR: an RNA-binding domain in transcription antitermination regulatory proteins. Trends Biochem. Sci. 27 (2002), 3–5.
171. [171] Romeo, T., Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol. Microbiol. 29 (1998), 1321–1330.
172. [172] Liu, M.Y., Gui, G., Wei, B., Preston, J.F. III, Oakford, L., Yuksel, U., Giedroc, D.P., Romeo, T., The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem. 272 (1997), 17,502–17,510.
173. [173] Djordjevic, S., Goudreau, P.N., Xu, Q., Stock, A.M., West, A.H., Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 1381–1386.
174. [174] West, A.H., Martinez-Hackert, E., Stock, A.M., Crystal structure of the catalytic domain of the chemotaxis receptor methylesterase, CheB. J. Mol. Biol. 250 (1995), 276–290.
175. [175] Aldridge, P., Paul, R., Goymer, P., Rainey, P., Jenal, U., Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol. Microbiol. 47 (2003), 1695–1708.
176. [176] Hecht, G.B., Newton, A., Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus. J. Bacteriol. 177 (1995), 6223–6229.
177. [177] Chan, C., Paul, R., Samoray, D., Amiot, N.C., Giese, B., Jenal, U., Schirmer, T., Structural basis of activity and allosteric control of diguanylate cyclase. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 17,084–17,089.
178. [178] Tamayo, R., Tischler, A.D., Camilli, A., The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280 (2005), 33,324–33,330.
179. [179] Ryan, R.P., Fouhy, Y., Lucey, J.F., Crossman, L.C., Spiro, S., He, Y.W., Zhang, L.H., Heeb, S., Camara, M., Williams, P., Dow, J.M., Cell–cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 6712–6717.
180. [180] Paul, R., Weiser, S., Amiot, N.C., Chan, C., Schirmer, T., Giese, B., Jenal, U., Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18 (2004), 715–727.
181. [181] Ryjenkov, D.A., Tarutina, M., Moskvin, O.V., Gomelsky, M., Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187 (2005), 1792–1798.
182. [182] Schmidt, A.J., Ryjenkov, D.A., Gomelsky, M., The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187 (2005), 4774–4781.
183. [183] Tischler, A.D., Camilli, A., Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53 (2004), 857–869.
184. [184] Kennelly, P.J., Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. FEMS Microbiol. Lett. 206 (2002), 1–8.
185. [185] Szurmant, H., Muff, T.J., Ordal, G.W., Bacillus subtilis CheC and FliY are members of a novel class of CheY-P-hydrolyzing proteins in the chemotactic signal transduction cascade. J. Biol. Chem. 279 (2004), 21,787–21,792.
186. [186] Karatan, E., Saulmon, M.M., Bunn, M.W., Ordal, G.W., Phosphorylation of the response regulator CheV is required for adaptation to attractants during Bacillus subtilis chemotaxis. J. Biol. Chem. 276 (2001), 43,618–43,626.
187. [187] Mitchell, S.L., Ismail, A.M., Kenrick, S.A., Camilli, A., The VieB auxiliary protein negatively regulates the VieSA signal transduction system in Vibrio cholerae. BMC Microbiol., 15, 2015, 59.