Prokaryotic 2-component systems and the ompr/phob superfamily

Canadian Journal of Microbiology

Volumn 61, Issue 11, 2015, Pages 799-810

  Nguyen, Minh Phuong ^a   Yoon, Joo Mi ^a   Cho, Man Ho ^a   Lee, Sang Won ^a  

^a Kyung Hee University   (South Korea)

Author keywords

2 component system; Bacterial signal transduction; OmpR PhoB family. M. P; Response regulator

Indexed keywords

BACTERIAL PROTEIN; OUTER MEMBRANE PROTEIN REGULATOR; PHOB PROTEIN; PROTEIN HISTIDINE KINASE; REC DOMAIN; RESPONSE REGULATOR; UNCLASSIFIED DRUG; WHTH EFFECTOR DOMAIN; DNA; OSMOLARITY RESPONSE REGULATOR PROTEINS; PHOB PROTEIN, BACTERIA; PROTEIN BINDING; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE; TRANSACTIVATOR PROTEIN;

AMINO ACID; BACTERIUM; CELLS AND CELL COMPONENTS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; MICROBIAL ACTIVITY; PROKARYOTE; PROTEIN;

AMINO TERMINAL SEQUENCE; BACTERIAL GENOME; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DIMERIZATION; DNA BINDING; GENE EXPRESSION; NONHUMAN; OLIGOMERIZATION; PHOSPHORELAY; PHOSPHORYLATION; PHOSPHOTRANSMISSION; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TWO COMPONENT REGULATORY SYSTEM; BACILLUS SUBTILIS; CELL MEMBRANE; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); PROKARYOTA;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL MEMBRANE; DNA; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 84945389059     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/cjm-2015-0345     Document Type: Review

References (128)

1. Alix, E., and Blanc-Potard, A.B. 2009. Hydrophobic peptides: novel regulators within bacterial membrane. Mol. Microbiol. 72(1): 5-11. doi:10.1111/j.1365-2958.2009.06626.x. PMID:19210615.
2. Aoyama, T., and Oka, A. 1990. A common mechanism of transcriptional activation by the three positive regulators, VirG, PhoB, and OmpR. FEBS Lett. 263(1): 1-4. doi:10.1016/0014-5793(90)80691-B. PMID:2185030.
3. Appleby, J.L., Parkinson, J.S., and Bourret, R.B. 1996. Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell, 86(6): 845-848. doi:10.1016/S0092-8674(00)80158-0. PMID:8808618.
4. Bachhawat, P., Swapna, G.V., Montelione, G.T., and Stock, A.M. 2005. Mechanism of activation for transcription factor PhoB suggested by different modes of dimerization in the inactive and active states. Structure, 13(9): 1353-1363. doi:10.1016/j.str. 2005.06.006. PMID:16154092.
5. Baikalov, I., Schroder, I., Kaczor-Grzeskowiak, M., Grzeskowiak, K., Gunsalus, R.P., and Dickerson, R.E. 1996. Structure of the Escherichia coli response regulator NarL. Biochemistry, 35(34): 11053-11061. doi:10.1021/bi960919o. PMID: 8780507.
6. Barakat, M., Ortet, P., Jourlin-Castelli, C., Ansaldi, M., Mejean, V., and Whitworth, D.E. 2009. P2CS: a two-component system resource for prokaryotic signal transduction research. BMC Genomics, 10: 315. doi:10.1186/1471-2164-10-315. PMID:19604365.
7. Barakat, M., Ortet, P., and Whitworth, D.E. 2011. P2CS: a database of prokaryotic two-component systems. Nucleic Acids Res. 39(Database issue): D771-D776. doi:10.1093/nar/gkq1023. PMID:21051349.
8. Barbieri, C.M., Wu, T., and Stock, A.M. 2013. Comprehensive analysis of OmpR phosphorylation, dimerization, and DNA binding supports a canonical model for activation. J. Mol. Biol. 425(10): 1612-1626. doi:10.1016/j.jmb.2013.02.003. PMID: 23399542.
9. Barta, M.L., Hickey, J.M., Anbanandam, A., Dyer, K., Hammel, M., and Hefty, P.S. 2014. Atypical response regulator ChxR from Chlamydia trachomatis is structurally poised for DNAbinding.PLoSOne,9(3):e91760.doi:10.1371/journal.pone. 0091760. PMID:24646934.
10. Batchelor, E., and Goulian, M. 2003. Robustness and the cycle of phosphorylation and dephosphorylation in a twocomponent regulatory system. Proc. Natl. Acad. Sci. U.S.A. 100(2): 691-696. doi:10.1073/pnas.0234782100. PMID:12522261.
11. Bell, C.H., Porter, S.L., Strawson, A., Stuart, D.I., and Armitage, J.P. 2010. Using structural information to change the phosphotransfer specificity of a two-component chemotaxis signalling complex. PLoS Biol. 8(2): e1000306. doi:10.1371/journal.pbio.1000306. PMID:20161720.
12. 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(12): 1505-1515. doi:10.1016/S0969-2126(00)88341-0. PMID:10647181.
13. Blanco, A.G., Sola, M., Gomis-Ruth, F.X., and Coll, M. 2002. Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure, 10(5): 701-713. doi:10.1016/S0969-2126(02)00761-X. PMID:12015152.
14. Bourret, R.B. 2010. Receiver domain structure and function in response regulator proteins. Curr. Opin. Microbiol. 13(2): 142-149. doi:10.1016/j.mib.2010.01.015. PMID:20211578.
15. Brennan, R.G. 1993. The winged-helix DNA-binding motif: anotherhelix-turn-helix takeoff. Cell,74(5): 773-776. doi:10.1016/0092-8674(93)90456-Z. PMID:8374950.
16. Buckler, D.R., Zhou, Y., and Stock, A.M. 2002. Evidence of intradomain and interdomain flexibility in an OmpR/PhoB homolog from Thermotoga maritima. Structure, 10(2): 153-164. doi:10.1016/S0969-2126(01)00706-7. PMID:11839301.
17. Buelow, D.R., and Raivio, T.L. 2010. Three (and more) component regulatory systems — auxiliary regulators of bacterial histidine kinases. Mol. Microbiol. 75(3): 547-566. doi:10.1111/j.1365-2958.2009.06982.x. PMID:19943903.
18. Cai, S.J., and Inouye, M. 2003. Spontaneous subunit exchange and biochemical evidence for trans-autophosphorylation in a dimer of Escherichia coli histidine kinase (EnvZ). J. Mol. Biol. 329(3): 495-503. doi:10.1016/S0022-2836(03)00446-7. PMID: 12767831.
19. Cameron, A.D., and Dorman, C.J. 2012. A fundamental regulatory mechanism operating through OmpR and DNA topology controls expression of Salmonella pathogenicity islands SPI-1 andSPI-2. PLoSGenet.8(3):e1002615.doi:10.1371/journal.pgen.1002615. PMID:22457642.
20. Capra, E.J., and Laub, M.T. 2012. Evolution of two-component signal transduction systems. Annu. Rev. Microbiol. 66: 325-347. doi:10.1146/annurev-micro-092611-150039. PMID:22746333.
21. Capra, E.J., Perchuk, B.S., Lubin, E.A., Ashenberg, O., Skerker, J.M., and Laub, M.T. 2010. Systematic dissection and trajectory-scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways. PLoS Genet. 6(11): e1001220. doi:10.1371/journal.pgen.1001220. PMID:21124821.
22. Capra, E.J., Perchuk, B.S., Skerker, J.M., and Laub, M.T. 2012. Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell, 150(1): 222-232. doi:10.1016/j.cell.2012.05.033. PMID:22770222.
23. Casino, P., Rubio, V., and Marina, A. 2009. Structural insight into partner specificity and phosphoryl transfer in twocomponent signal transduction. Cell, 139(2): 325-336. doi:10. 1016/j.cell.2009.08.032. PMID:19800110.
24. Chen, Y., Abdel-Fattah, W.R., and Hulett, F.M. 2004. Residues required for Bacillus subtilis PhoP DNA binding or RNA polymerase interaction: alanine scanning of PhoP effector domain transactivation loop and alpha helix 3. J. Bacteriol. 186(5): 1493-1502. doi:10.1128/JB.186.5.1493-1502.2004. PMID: 14973033.
25. Cho, H.S., Lee, S.-Y., Yan, D., Pan, X., Parkinson, J.S., Kustu, S., et al. 2000. NMR structure of activated CheY. J. Mol. Biol. 297(3): 543-551. doi:10.1006/jmbi.2000.3595. PMID:10731410.
26. Clark, K.L., Halay, E.D., Lai, E., and Burley, S.K. 1993. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature, 364(6436): 412-420. doi:10.1038/364412a0. PMID:8332212.
27. Clubb, R.T., Omichinski, J.G., Savilahti, H., Mizuuchi, K., Gronenborn, A.M., and Clore, G.M. 1994. A novel class of winged helix-turn-helix protein: the DNA-binding domain of Mu transposase. Structure, 2(11): 1041-1048. doi:10.1016/S0969-2126(94)00107-3. PMID:7881904.
28. Cock, P.J., and Whitworth, D.E. 2007. Evolution of prokaryotic two-component system signaling pathways: gene fusions and fissions. Mol. Biol. Evol. 24(11): 2355-2357. doi:10.1093/molbev/msm170. PMID:17709334.
29. Creager-Allen, R.L., Silversmith, R.E., and Bourret, R.B. 2013. A link between dimerization and autophosphorylation of the response regulator PhoB. J. Biol. Chem. 288(30): 21755-21769. doi:10.1074/jbc.M113.471763. PMID:23760278. De la
30. Cruz, M.A., and Calva, E. 2010. The complexities of porin genetic regulation. J. Mol. Microbiol. Biotechnol. 18(1): 24-36. doi:10.1159/000274309. PMID:20068355.
31. Debnath, I., Norton, J.P., Barber, A.E., Ott, E.M., Dhakal, B.K., Kulesus, R.R., and Mulvey, M.A. 2013. The Cpx stress response system potentiates the fitness and virulence of uropathogenic Escherichia coli. Infect. Immun. 81(5): 1450-1459. doi:10.1128/IAI.01213-12. PMID:23429541.
32. Delany, I., Spohn, G., Rappuoli, R., and Scarlato, V. 2002. Growth phase-dependent regulation of target gene promoters for binding of the essential orphan response regulator HP1043 of Helicobacter pylori. J. Bacteriol. 184(17): 4800-4810. doi:10.1128/JB.184.17.4800-4810.2002. PMID:12169605.
33. 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. U.S.A. 95(4): 1381-1386. doi:10.1073/pnas.95.4.1381. PMID:9465023.
34. Dutta, R., and Inouye, M. 1996. Reverse phosphotransfer from OmpR to EnvZ in a kinase/phosphatase mutant of EnvZ (EnvZN347D), a bifunctional signal transducer of Escherichia coli. J. Biol. Chem. 271(3): 1424-1429. doi:10.1074/jbc.271.3. 1424. PMID:8576133.
35. Espinosa, J., Lopez-Redondo, M.L., Miguel-Romero, L., Neira, J.L., Marina, A., and Contreras, A. 2012. Insights into the mechanism of activation of the phosphorylation-independent response regulator NblR. Role of residues Cys69 and Cys96. Biochim. Biophys. Acta, 1819(5): 382-390. doi:10.1016/j.bbagrm.2012.01.007. PMID:22306661.
36. Fabret, C., Feher, V.A., and Hoch, J.A. 1999. Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J. Bacteriol. 181(7): 1975-1983. PMID:10094672.
37. Feng, J., Atkinson, M.R., McCleary, W., Stock, J.B., Wanner, B.L., and Ninfa, A.J. 1992. Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli. J. Bacteriol. 174(19): 6061-6070. PMID:1356964.
38. Fisher, S.L., Jiang, W., Wanner, B.L., and Walsh, C.T. 1995. Crosstalk 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(39): 23143-23149. doi:10.1074/jbc.270.39. 23143. PMID:7559459.
39. Fleischer, R., Heermann, R., Jung, K., and Hunke, S. 2007. Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J. Biol. Chem. 282(12): 8583-8593. doi:10.1074/jbc.M605785200. PMID:17259177.
40. Friedland, N., Mack, T.R., Yu, M., Hung, L.W., Terwilliger, T.C., Waldo, G.S., and Stock, A.M. 2007. Domain orientation in the inactive response regulator Mycobacterium tuberculosis MtrA provides a barrier to activation. Biochemistry, 46(23): 6733-6743. doi:10.1021/bi602546q. PMID:17511470.
41. Galperin, M.Y. 2006. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol. 188(12): 4169-4182. doi:10.1128/JB.01887-05. PMID:16740923.
42. Galperin, M.Y. 2010. Diversity of structure and function of response regulator output domains. Curr. Opin. Microbiol. 13(2): 150-159. doi:10.1016/j.mib.2010.01.005. PMID:20226724.
43. Gao, R., and Stock, A.M. 2009. Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63: 133-154. doi:10.1146/annurev.micro.091208.073214. PMID:19575571.
44. Gao, R., and Stock, A.M. 2013. Probing kinase and phosphatase activities of two-component systems in vivo with concentrationdependent phosphorylation profiling. Proc. Natl. Acad. Sci. U.S.A. 110(2): 672-677. doi:10.1073/pnas.1214587110. PMID:23267085.
45. Gao, R., Mack, T.R., and Stock, A.M. 2007. Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem. Sci. 32(5): 225-234. doi:10.1016/j.tibs.2007.03.002. PMID:17433693.
46. Gao, R., Tao, Y., and Stock, A.M. 2008. System-level mapping of Escherichia coli response regulator dimerization with FRET hybrids. Mol. Microbiol.69(6): 1358-1372. doi:10.1111/j.1365-2958.2008.06355.x. PMID:18631241.
47. Grebe, T.W., and Stock, J.B. 1999. The histidine protein kinase superfamily. Adv. Microb. Physiol. 41: 139-227. doi:10.1016/S0065-2911(08)60167-8. PMID:10500846.
48. Gupta, S., Sinha, A., and Sarkar, D. 2006. Transcriptional autoregulation by Mycobacterium tuberculosis PhoP involves recognition of novel direct repeat sequences in the regulatory region of the promoter. FEBS Lett. 580(22): 5328-5338. doi:10.1016/j.febslet.2006.09.004. PMID:16979633.
49. Halkides, C.J., McEvoy, M.M., Casper, E., Matsumura, P., Volz, K., and Dahlquist, F.W. 2000. The 1.9 Å resolution crystal structure of phosphono-CheY, an analogue of the active form of the response regulator, CheY. Biochemistry, 39(18): 5280-5286. doi:10.1021/bi9925524. PMID:10819997.
50. Harrison, C.J., Bohm, A.A., and Nelson, H.C. 1994. Crystal structure of the DNA binding domain of the heat shock transcription factor. Science, 263(5144): 224-227. doi:10.1126/science.8284672. PMID:8284672.
51. Hess, J.F., Oosawa, K., Kaplan, N., and Simon, M.I. 1988. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell, 53(1): 79-87. doi:10.1016/0092-8674(88)90489-8. PMID:3280143.
52. Hickey, J.M., Lovell, S., Battaile, K.P., Hu, L., Middaugh, C.R., and Hefty, P.S. 2011. The atypical response regulator protein ChxR has structural characteristics and dimer interface interactions that are unique within the OmpR/PhoB subfamily. J. Biol. Chem. 286(37): 32606-32616. doi:10.1074/jbc.M111.220574. PMID:21775428.
53. Hong, E., Lee, H.M., Ko, H., Kim, D.U., Jeon, B.Y., Jung, J., et al. 2007. Structure of an atypical orphan response regulator protein supports a new phosphorylation-independent regulatory mechanism. J. Biol. Chem. 282(28): 20667-20675. doi:10.1074/jbc.M609104200. PMID:17491010.
54. Howell, A., Dubrac, S., Andersen, K.K., Noone, D., Fert, J., Msadek, T., and Devine, K. 2003. Genes controlled by the essential YycG/YycF two-component system of Bacillus subtilis revealed through a novel hybrid regulator approach. Mol. Microbiol. 49(6): 1639-1655. doi:10.1046/j.1365-2958.2003.03661.x. PMID:12950927.
55. Hsing, W., Russo, F.D., Bernd, K.K., and Silhavy, T.J. 1998. Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ. J. Bacteriol. 180(17): 4538-4546. PMID:9721293.
56. Jeon, Y., Lee, Y.S., Han, J.S., Kim, J.B., and Hwang, D.S. 2001. Multimerization of phosphorylated and non-phosphorylated ArcA is necessary for the response regulator function of the Arc twocomponent signal transduction system. J. Biol. Chem. 276(44): 40873-40879. doi:10.1074/jbc.M104855200. PMID:11527965.
57. Jiang, M., Shao, W.L., Perego, M., and Hoch, J.A. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38(3): 535-542. doi:10.1046/j.1365-2958.2000.02148.x. PMID:11069677.
58. Kato, A., and Groisman, E.A. 2004. Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev. 18(18): 2302-2313. doi:10.1101/gad.1230804. PMID: 15371344.
59. Kern, D., Volkman, B.F., Luginbuhl, P., Nohaile, M.J., Kustu, S., and Wemmer, D.E. 1999. Structure of a transiently phosphorylated switch in bacterial signal transduction. Nature, 402(6764): 894-898. doi:10.1038/47273. PMID:10622255.
60. King-Scott, J., Nowak, E., Mylonas, E., Panjikar, S., Roessle, M., Svergun, D.I., and Tucker, P.A. 2007. The structure of a fulllength response regulator from Mycobacterium tuberculosis in a stabilized three-dimensional domain-swapped, activated state. J. Biol. Chem. 282(52): 37717-37729. doi:10.1074/jbc.M705081200. PMID:17942407.
61. Koo, I.C., Walthers, D., Hefty, P.S., Kenney, L.J., and Stephens, R.S. 2006. ChxR is a transcriptional activator in Chlamydia. Proc. Natl. Acad. Sci. U.S.A. 103(3): 750-755. doi:10.1073/pnas.0509690103. PMID:16407127.
62. Koshland, D.E., Jr. 1977. A response regulator model in a simple sensory system. Science, 196(4294): 1055-1063. doi:10.1126/science.870969. PMID:870969.
63. Kwon, E., Kim, D.Y., Ngo, T.D., Gross, C.A., Gross, J.D., and Kim, K.K. 2012. The crystal structure of the periplasmic domain of Vibrio parahaemolyticus CpxA. Protein Sci. 21(9): 1334-1343. doi:10.1002/pro.2120. PMID:22760860.
64. Lai, E., Prezioso, V.R., Tao, W.F., Chen, W.S., and Darnell, J.E. 1991. Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 5(3): 416-427. doi:10.1101/gad.5.3.416. PMID:1672118.
65. Laub, M.T., and Goulian, M. 2007. Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41: 121-145. doi:10.1146/annurev.genet.41.042007.170548. PMID:18076326.
66. 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. Nat. Struct. Biol. 8(1): 52-56. doi:10.1038/83053. PMID:11135671.
67. Lewis, R.J., Brannigan, J.A., Muchova, K., Barak, I., and Wilkinson, A.J. 1999. Phosphorylated aspartate in the structure of a response regulator protein. J. Mol. Biol. 294(1): 9-15. doi:10.1006/jmbi.1999.3261.
68. Lin, W., Wang, Y., Han, X.B., Zhang, Z.L., Wang, C.Y., Wang, J., et al. 2014. Atypical OmpR/PhoB subfamily response regulator GlnR of actinomycetes functions as a homodimer, stabilized by the unphosphorylated conserved Asp-focused charge interactions. J. Biol. Chem. 289(22): 15413-15425. doi: 10.1074/jbc.M113.543504. PMID:24733389.
69. Liu, G., Chater, K.F., Chandra, G., Niu, G., and Tan, H. 2013. Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol. Mol. Biol. Rev. 77(1): 112-143. doi:10.1128/MMBR.00054-12. PMID:23471619.
70. Liu, Y., Gao, Z.Q., She, Z., Qu, K., Wang, W.J., Shtykova, E.V., et al. 2012. The structural basis of the response regulator DrRRA from Deinococcus radiodurans. Biochem. Biophys. Res. Commun. 417(4): 1206-1212. doi:10.1016/j.bbrc.2011.12.110. PMID:22227191.
71. Lukat, G.S., McCleary, W.R., Stock, A.M., and Stock, J.B. 1992. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci. U.S.A. 89(2): 718-722. doi:10.1073/pnas.89.2.718. PMID: 1731345.
72. Martinez-Hackert, E., and Stock, A.M. 1997a. The DNA-binding domain of OmpR: crystal structures of a winged helix transcription factor. Structure, 5(1): 109-124. doi:10.1016/S0969-2126(97)00170-6. PMID:9016718.
73. Martinez-Hackert, E., and Stock, A.M. 1997b. Structural relationships in the OmpR family of winged-helix transcription factors. J. Mol. Biol. 269(3): 301-312. doi:10.1006/jmbi.1997.1065. PMID:9199401.
74. Matsubara, M., Kitaoka, S., Takeda, S., and Mizuno, T. 2000. Tuning of the porin expression under anaerobic growth conditions by His-to-Asp cross-phosphorelay through both the EnvZ-osmosensor and ArcB-anaerosensor in Escherichia coli. Genes Cells, 5(7): 555-569. doi:10.1046/j.1365-2443.2000.00347.x. PMID:10947842.
75. Mattison, K., Oropeza, R., and Kenney, L.J. 2002. The linker region plays an important role in the interdomain communication of the response regulator OmpR. J. Biol. Chem. 277(36): 32714-32721. doi:10.1074/jbc.M204122200. PMID:12077136.
76. Menon, S., and Wang, S. 2011. Structure of the response regulator PhoP from Mycobacterium tuberculosis reveals a dimer through the receiver domain. Biochemistry, 50(26): 5948-5957. doi:10.1021/bi2005575. PMID:21634789.
77. Mitrophanov, A.Y., and Groisman, E.A. 2008. Signal integration in bacterial two-component regulatory systems. Genes Dev. 22(19): 2601-2611. doi:10.1101/gad.1700308. PMID:18832064.
78. Narayanan, A., Paul, L.N., Tomar, S., Patil, D.N., Kumar, P., and Yernool, D.A. 2012. Structure-function studies of DNA binding domain of response regulator KdpE reveals equal affinity interactions at DNA half-sites. PLoS One, 7(1): e30102. doi:10. 1371/journal.pone.0030102. PMID:22291906.
79. Ninfa, E.G., Atkinson, M.R., Kamberov, E.S., and Ninfa, A.J. 1993. Mechanism of autophosphorylation of Escherichia coli nitrogen regulator II (NRII or NtrB): trans-phosphorylation between subunits. J. Bacteriol. 175(21): 7024-7032. PMID:8226644.
80. Nixon, B.T., Ronson, C.W., and Ausubel, F.M. 1986. Twocomponent regulatory systems responsive to environmental stimuli share strongly conserved domains with the nitrogen assimilation regulatory genes ntrB and ntrC. Proc. Natl. Acad. Sci. U.S.A. 83(20): 7850-7854. doi:10.1073/pnas.83.20.7850. PMID:3020561.
81. Novak, R., Henriques, B., Charpentier, E., Normark, S., and Tuomanen, E. 1999. Emergence of vancomycin tolerance in Streptococcus pneumoniae. Nature, 399(6736): 590-593. doi:10.1038/21202. PMID:10376600.
82. Nowak, E., Panjikar, S., Konarev, P., Svergun, D.I., and Tucker, P.A. 2006. The structural basis of signal transduction for the response regulator PrrA from Mycobacterium tuberculosis. J. Biol. Chem. 281(14): 9659-9666. doi:10.1074/jbc.M512004200. PMID:16434396.
83. Parkinson, G., Wilson, C., Gunasekera, A., Ebright, Y.W., Ebright, R.E., and Berman, H.M. 1996. Structure of the CAP-DNA complex at 2.5 Å resolution: a complete picture of the protein-DNA interface. J. Mol. Biol. 260(3): 395-408. doi:10.1006/jmbi.1996.0409. PMID:8757802.
84. Parkinson, J.S., and Kofoid, E.C. 1992. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26(1): 71-112. doi:10.1146/annurev.ge.26.120192.000443. PMID:1482126.
85. Pelton, J.G., Kustu, S., and Wemmer, D.E. 1999. Solution structure of the DNA-binding domain of NtrC with three alanine substitutions. J. Mol. Biol. 292(5): 1095-1110. doi:10.1006/jmbi.1999.3140. PMID:10512705
86. Pena-Sandoval, G.R., and Georgellis, D. 2010. The ArcB sensor kinase of Escherichia coli autophosphorylates by an intramolecular reaction. J. Bacteriol. 192(6): 1735-1739. doi:10.1128/JB.01401-09. PMID:20097862.
87. Perraud, A.L., Weiss, V., and Gross, R. 1999. Signalling pathways in two-component phosphorelay systems. Trends Microbiol. 7(3): 115-120. doi:10.1016/S0966-842X(99)01458-4. PMID: 10203840.
88. Podgornaia, A.I., and Laub, M.T. 2013. Determinants of specificity in two-component signal transduction. Curr. Opin. Microbiol. 16(2): 156-162. doi:10.1016/j.mib.2013.01.004. PMID:23352354.
89. Pontiggia, F., Pachov, D.V., Clarkson, M.W., Villali, J., Hagan, M.F., Pande, V.S., and Kern, D. 2015. Free energy land-scape of activation in a signalling protein at atomic resolution. Nat. Commun. 6: 7284. doi:10.1038/ncomms8284. PMID: 26073309.
90. Qin, L., Yoshida, T., and Inouye, M. 2001. The critical role of DNA in the equilibrium between OmpR and phosphorylated OmpR mediated by EnvZ in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 98(3): 908-913. doi:10.1073/pnas.98.3.908. PMID: 11158569.
91. Quinn, H.J., Cameron, A.D., and Dorman, C.J. 2014. Bacterial regulon evolution: distinct responses and roles for the identical OmpR proteins of Salmonella typhimurium and Escherichia coli in the acid stress response. PLoS Genet. 10(3): e1004215. doi:10.1371/journal.pgen.1004215. PMID:24603618.
92. Ramakrishnan, V., Finch, J.T., Graziano, V., Lee, P.L., and Sweet, R.M. 1993. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature, 362(6417): 219-223. doi:10.1038/362219a0. PMID: 8384699.
93. Rhee, J.E., Sheng, W., Morgan, L.K., Nolet, R., Liao, X., and Kenney, L.J. 2008. Amino acids important for DNA recognition by the response regulator OmpR. J. Biol. Chem. 283(13): 8664-8677. doi:10.1074/jbc.M705550200. PMID:18195018.
94. Ritzefeld, M., Walhorn, V., Anselmetti, D., and Sewald, N. 2013. Analysis of DNA interactions using single-molecule force spectroscopy. Amino Acids, 44(6): 1457-1475. doi:10.1007/s00726-013-1474-4. PMID:23468137.
95. Robinson, V.L., Wu, T., and Stock, A.M. 2003. Structural analysis of the domain interface in DrrB, a response regulator of the OmpR/PhoB subfamily. J. Bacteriol. 185(14): 4186-4194. doi: 10.1128/JB.185.14.4186-4194.2003. PMID:12837793.
96. Rowland, M.A., and Deeds, E.J. 2014. Crosstalk and the evolution of specificity in two-component signaling. Proc. Natl. Acad. Sci. U.S.A. 111(15): 5550-5555. doi:10.1073/pnas.1317178111. PMID:24706803.
97. Ruiz, D., Salinas, P., Lopez-Redondo, M.L., Cayuela, M.L., Marina, A., and Contreras, A. 2008. Phosphorylation-independent activation of the atypical response regulator NblR. Microbiology, 154(10): 3002-3015. doi:10.1099/mic.0.2008/020677-0. PMID: 18832306.
98. Schaller, G.E., Shiu, S.H., and Armitage, J.P. 2011. Twocomponent systems and their co-option for eukaryotic signal transduction. Curr. Biol. 21(9): R320-R330. doi:10.1016/j.cub.2011.02.045. PMID:21549954.
99. Schultz, S.C., Shields, G.C., and Steitz, T.A. 1991. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science, 253(5023): 1001-1007. doi:10.1126/science.1653449. PMID:1653449.
100. Sidote, D.J., Barbieri, C.M., Wu, T., and Stock, A.M. 2008. Structure of the Staphylococcus aureus AgrA LytTR domain bound to DNA reveals a beta fold with an unusual mode of binding. Structure, 16(5): 727-735. doi:10.1016/j.str.2008.02.011. PMID: 18462677.
101. Simon, G., Jourlin, C., Ansaldi, M., Pascal, M.C., Chippaux, M., and Mejean, V. 1995. Binding of the TorR regulator to cisacting direct repeats activates tor operon expression. Mol. Microbiol. 17(5): 971-980. doi:10.1111/j.1365-2958.1995.mmi_17050971.x. PMID:8596446.
102. Simon, M.I., Borkovich, K.A., Bourret, R.B., and Hess, J.F. 1989. Protein phosphorylation in the bacterial chemotaxis system. Biochimie, 71(9-10): 1013-1019. doi:10.1016/0300-9084(89) 90105-3. PMID:2512992.
103. Sinha, A., Gupta, S., Bhutani, S., Pathak, A., and Sarkar, D. 2008. PhoP-PhoP interaction at adjacent PhoP binding sites is influenced by protein phosphorylation. J. Bacteriol. 190(4): 1317-1328. doi:10.1128/JB.01074-07. PMID:18065544.
104. Siryaporn, A., and Goulian, M. 2008. Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli. Mol. Microbiol. 70(2): 494-506. doi:10.1111/j.1365-2958.2008.06426.x. PMID:18761686.
105. Skerker, J.M., Prasol, M.S., Perchuk, B.S., Biondi, E.G., and Laub, M.T. 2005. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol. 3(10): e334. doi:10.1371/journal.pbio.0030334. PMID:16176121.
106. Skerker, J.M., Perchuk, B.S., Siryaporn, A., Lubin, E.A., Ashenberg, O., Goulian, M., and Laub, M.T. 2008. Rewiring the specificity of two-component signal transduction systems. Cell, 133(6): 1043-1054. doi:10.1016/j.cell.2008.04.040. PMID:18555780.
107. Stock, A.M., Mottonen, J.M., Stock, J.B., and Schutt, C.E. 1989. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature, 337(6209): 745-749. doi:10.1038/337745a0. PMID:2645526.
108. Stock, A.M., Robinson, V.L., and Goudreau, P.N. 2000. Twocomponent signal transduction. Annu. Rev. Biochem. 69(1): 183-215. doi:10.1146/annurev.biochem.69.1.183. PMID:10966457.
109. Stock, J.B., Ninfa, A.J., and Stock, A.M. 1989. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53(4): 450-490. PMID:2556636.
110. Toro-Roman, A., Mack, T.R., and Stock, A.M. 2005a. Structural analysis and solution studies of the activated regulatory domain of the response regulator ArcA: a symmetric dimer mediated by the α4-α5-α5 face. J. Mol. Biol. 349(1): 11-26. doi: 10.1016/j.jmb.2005.03.059. PMID:15876365.
111. Toro-Roman, A., Wu, T., and Stock, A.M. 2005b. A common dimerization interface in bacterial response regulators KdpE and TorR. Protein Sci. 14(12): 3077-3088. doi:10.1110/ps. 051722805. PMID:16322582.
112. Trajtenberg, F., Albanesi, D., Ruetalo, N., Botti, H., Mechaly, A.E., Nieves, M., et al. 2014. Allosteric activation of bacterial response regulators: the role of the cognate histidine kinase beyond phosphorylation. mBio, 5(6): e02105. doi: 10.1128/mBio.02105-14. PMID:25406381.
113. Ulrich, L.E., and Zhulin, I.B. 2010. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res. 38(Database issue): D401-D407. doi: 10.1093/nar/gkp940. PMID:19900966.
114. Ulrich, L.E., Koonin, E.V., and Zhulin, I.B. 2005. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13(2): 52-56. doi:10.1016/j.tim.2004.12.006. PMID:15680762.
115. Vanatta, D.K., Shukla, D., Lawrenz, M., and Pande, V.S. 2015. A network of molecular switches controls the activation of the two-component response regulator NtrC. Nat. Commun. 6: 7283. doi:10.1038/ncomms8283. PMID:26073186.
116. Villali, J., Pontiggia, F., Clarkson, M.W., Hagan, M.F., and Kern, D. 2014. Evidence against the “Y-T coupling” mechanism of activation in the response regulator NtrC. J. Mol. Biol. 426(7): 1554-1567. doi:10.1016/j.jmb.2013.12.027. PMID: 24406745.
117. Vogel, J., and Papenfort, K. 2006. Small non-coding RNAs and the bacterial outer membrane. Curr. Opin. Microbiol. 9(6): 605-611. doi:10.1016/j.mib.2006.10.006. PMID:17055775.
118. Volkman, B.F., Lipson, D., Wemmer, D.E., and Kern, D. 2001. Two-state allosteric behavior in a single-domain signaling protein. Science, 291(5512): 2429-2433. doi:10.1126/science.291.5512.2429. PMID:11264542.
119. Walthers, D., Tran, V.K., and Kenney, L.J. 2003. Interdomain linkers of homologous response regulators determine their mechanism of action. J. Bacteriol. 185(1): 317-324. doi:10.1128/JB.185.1.317-324.2003. PMID:12486069.
120. Wang, L., Tian, X., Wang, J., Yang, H., Fan, K., Xu, G., et al. 2009. Autoregulation of antibiotic biosynthesis by binding of the end product to an atypical response regulator. Proc. Natl. Acad. Sci. U.S.A. 106(21): 8617-8622. doi:10.1073/pnas.0900592106. PMID:19423672.
121. Wanner, B.L. 1993. Gene regulation by phosphate in enteric bacteria. J. Cell. Biochem. 51(1): 47-54. doi:10.1002/jcb.240510110. PMID:8432742.
122. Weigt, M., White, R.A., Szurmant, H., Hoch, J.A., and Hwa, T. 2009. Identification of direct residue contacts in protein-protein interaction by message passing. Proc. Natl. Acad. Sci. U.S.A. 106(1): 67-72. doi:10.1073/pnas.0805923106. PMID:19116270.
123. West, A.H., and Stock, A.M. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26(6): 369-376. doi:10.1016/S0968-0004(01)01852-7. PMID:11406410.
124. West, A.H., Martinez-Hackert, E., and Stock, A.M. 1995. Crystal structure of the catalytic domain of the chemotaxis receptor methylesterase, CheB. J. Mol. Biol. 250(2): 276-290. doi:10.1006/jmbi.1995.0376. PMID:7608974.
125. Whitworth, D.E. 2012. Classification and organization of twocomponent systems. In Two-component systems in bacteria. Horizon Scientific Press, Norfolk, UK. pp. 1-20.
126. Wilson, K.P., Shewchuk, L.M., Brennan, R.G., Otsuka, A.J., and Matthews, B.W. 1992. Escherichia coli biotin holoenzyme synthetase/ bio repressor crystal structure delineates the biotinand DNA-binding domains. Proc. Natl. Acad. Sci. U.S.A. 89(19): 9257-9261. doi:10.1073/pnas.89.19.9257. PMID:1409631.
127. Yamane, T., Okamura, H., Ikeguchi, M., Nishimura, Y., and Kidera, A. 2008. Water-mediated interactions between DNA and PhoB DNA-binding/transactivation domain: NMR-restrained molecular dynamics in explicit water environment. Proteins, 71(4): 1970-1983. doi:10.1002/prot.21874. PMID:18186481.
128. Zarrinpar, A., Park, S.H., and Lim, W.A. 2003. Optimization of specificity in a cellular protein interaction network by negative selection. Nature, 426(6967): 676-680. doi:10.1038/nature02178. PMID:14668868.