1932

Abstract

Perceiving environmental and internal information and reacting in adaptive ways are essential attributes of living organisms. Two-component systems are relevant protein machineries from prokaryotes and lower eukaryotes that enable cells to sense and process signals. Implicating sensory histidine kinases and response regulator proteins, both components take advantage of protein phosphorylation and flexibility to switch conformations in a signal-dependent way. Dozens of two-component systems act simultaneously in any given cell, challenging our understanding about the means that ensure proper connectivity. This review dives into the molecular level, attempting to summarize an emerging picture of how histidine kinases and cognate response regulators achieve required efficiency, specificity, and directionality of signaling pathways, properties that rely on protein:protein interactions. α helices that carry information through long distances, the fine combination of loose and specific kinase/regulator interactions, and malleable reaction centers built when the two components meet emerge as relevant universal principles.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-091018-054627
2019-09-08
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/73/1/annurev-micro-091018-054627.html?itemId=/content/journals/10.1146/annurev-micro-091018-054627&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Aakre CD, Herrou J, Phung TN, Perchuk BS, Crosson S, Laub MT 2015. Evolving new protein-protein interaction specificity through promiscuous intermediates. Cell 163:594–606
    [Google Scholar]
  2. 2. 
    Adebali O, Petukh MG, Reznik AO, Tishkov AV, Upadhyay AA, Zhulin IB 2017. Class III histidine kinases: a recently accessorized kinase domain in putative modulators of type IV pilus-based motility. J. Bacteriol. 199:e00218–17
    [Google Scholar]
  3. 3. 
    Albanesi D, Mansilla MC, de Mendoza D 2004. The membrane fluidity sensor DesK of Bacillus subtilis controls the signal decay of its cognate response regulator. J. Bacteriol. 186:2655–63
    [Google Scholar]
  4. 4. 
    Albanesi D, Martin M, Trajtenberg F, Mansilla MC, Haouz A et al. 2009. Structural plasticity and catalysis regulation of a thermosensor histidine kinase. PNAS 106:16185–90DesK structures in different conformations show experimentally that the DHp coiled-coil regulates HK activity.
    [Google Scholar]
  5. 5. 
    Alberty R. 2010. IUBMB-IUPAC Joint Commission on Biochemical Nomenclature (JCBN) recommendations for nomenclature and tables in biochemical thermodynamics. Handbook of Biochemistry and Molecular Biology R Lundblad, F Macdonald 537–50 Boca Raton, FL: CRC
    [Google Scholar]
  6. 6. 
    Anantharaman V, Balaji S, Aravind L 2006. The signaling helix: a common functional theme in diverse signaling proteins. Biol. Direct. 1:25
    [Google Scholar]
  7. 7. 
    Ashenberg O, Laub MT. 2013. Using analyses of amino acid coevolution to understand protein structure and function. Methods Enzymol 523:191–212
    [Google Scholar]
  8. 8. 
    Attwood PV. 2013. PN bond protein phosphatases. Biochim. Biophys. Acta Proteins Proteom. 1834:470–78
    [Google Scholar]
  9. 9. 
    Azeloglu EU, Iyengar R. 2015. Signaling networks: information flow, computation, and decision making. Cold Spring Harb. Perspect. Biol. 7:a005934
    [Google Scholar]
  10. 10. 
    Batchelor E, Goulian M. 2003. Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. PNAS 100:691–96
    [Google Scholar]
  11. 11. 
    Bell CH, Porter SL, Strawson A, Stuart DI, Armitage JP 2010. Using structural information to change the phosphotransfer specificity of a two-component chemotaxis signalling complex. PLOS Biol 8:e1000306
    [Google Scholar]
  12. 12. 
    Bennett B, Kimball E, Gao M, Osterhout R, Van Dien S, Rabinowitz J 2009. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol 5:593–99
    [Google Scholar]
  13. 13. 
    Berntsson O, Diensthuber RP, Panman MR, Bjorling A, Gustavsson E et al. 2017. Sequential conformational transitions and α-helical supercoiling regulate a sensor histidine kinase. Nat. Commun. 8:284Time-resolved in-solution techniques support left-handed coiled-coiling as a means of transmitting information in histidine kinases.
    [Google Scholar]
  14. 14. 
    Berntsson O, Diensthuber RP, Panman MR, Bjorling A, Hughes AJ et al. 2017. Time-resolved X-ray solution scattering reveals the structural photoactivation of a light-oxygen-voltage photoreceptor. Structure 25:933–38.e3
    [Google Scholar]
  15. 15. 
    Bhate MP, Molnar KS, Goulian M, DeGrado WF 2015. Signal transduction in histidine kinases: insights from new structures. Structure 23:981–94
    [Google Scholar]
  16. 16. 
    Bourret RB, Thomas SA, Page SC, Creager-Allen RL, Moore AM, Silversmith RE 2010. Measurement of response regulator autodephosphorylation rates spanning six orders of magnitude. Methods Enzymol 471:89–114
    [Google Scholar]
  17. 17. 
    Brown JH, Cohen C, Parry DAD 1996. Heptad breaks in α-helical coiled coils: stutters and stammers. Proteins 26:134–45
    [Google Scholar]
  18. 18. 
    Burbulys D, Trach KA, Hoch JA 1991. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64:545–52
    [Google Scholar]
  19. 19. 
    Cai SJ, Inouye M. 2002. EnvZ-OmpR interaction and osmoregulation in Escherichia coli. J. Biol. Chem 277:24155–61
    [Google Scholar]
  20. 20. 
    Capra EJ, Laub MT. 2012. Evolution of two-component signal transduction systems. Annu. Rev. Microbiol. 66:325–47
    [Google Scholar]
  21. 21. 
    Capra EJ, Perchuk BS, Ashenberg O, Seid CA, Snow HR et al. 2012. Spatial tethering of kinases to their substrates relaxes evolutionary constraints on specificity. Mol. Microbiol. 86:1393–403
    [Google Scholar]
  22. 22. 
    Capra EJ, Perchuk BS, Lubin EA, Ashenberg O, Skerker JM, Laub MT 2010. Systematic dissection and trajectory-scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways. PLOS Genet 6:e1001220
    [Google Scholar]
  23. 23. 
    Capra EJ, Perchuk BS, Skerker JM, Laub MT 2012. Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell 150:222–32
    [Google Scholar]
  24. 24. 
    Casino P, Miguel-Romero L, Marina A 2014. Visualizing autophosphorylation in histidine kinases. Nat. Commun. 5:3258
    [Google Scholar]
  25. 25. 
    Casino P, Rubio V, Marina A 2009. Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell 139:325–36This hallmark study uncovered the first crystal structure of a bona fide HK:RR complex from a hyperthermophile.
    [Google Scholar]
  26. 26. 
    Chamnongpol S, Cromie M, Groisman EA 2003. Mg2+ sensing by the Mg2+ sensor PhoQ of Salmonella enterica. J. Mol. Biol 325:795–807
    [Google Scholar]
  27. 27. 
    Cheung J, Hendrickson WA. 2009. Structural analysis of ligand stimulation of the histidine kinase NarX. Structure 17:190–201
    [Google Scholar]
  28. 28. 
    Cheung J, Hendrickson WA. 2010. Sensor domains of two-component regulatory systems. Curr. Opin. Microbiol. 13:116–23
    [Google Scholar]
  29. 29. 
    Cleland WW, Hengge AC. 2006. Enzymatic mechanisms of phosphate and sulfate transfer. Chem. Rev. 106:3252–78
    [Google Scholar]
  30. 30. 
    Cock PJ, Whitworth DE. 2007. Evolution of prokaryotic two-component system signaling pathways: gene fusions and fissions. Mol. Biol. Evol. 24:2355–57
    [Google Scholar]
  31. 31. 
    Crick F. 1953. The packing of α-helices: simple coiled-coils. Acta Crystallogr 6:689–97
    [Google Scholar]
  32. 32. 
    Davidson P, Eutsey R, Redler B, Hiller NL, Laub MT, Durand D 2018. Flexibility and constraint: evolutionary remodeling of the sporulation initiation pathway in Firmicutes. PLOS Genet 14:e1007470Phosphorelays, evolved from simpler systems, also suffer reductive evolution, implicating pathways’ remodeling and a richer specificity code.
    [Google Scholar]
  33. 33. 
    Diensthuber RP, Bommer M, Gleichmann T, Möglich A 2013. Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators. Structure 21:1127–36
    [Google Scholar]
  34. 34. 
    Dubey BN, Lori C, Ozaki S, Fucile G, Plaza-Menacho I et al. 2016. Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking. Sci. Adv. 2:e1600823
    [Google Scholar]
  35. 35. 
    Dutta R, Inouye M. 2000. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 25:24–28
    [Google Scholar]
  36. 36. 
    Engelhard C, Diensthuber RP, Möglich A, Bittl R 2017. Blue-light reception through quaternary transitions. Sci. Rep. 7:1385
    [Google Scholar]
  37. 37. 
    Fassler JS, West AH. 2013. Histidine phosphotransfer proteins in fungal two-component signal transduction pathways. Eukaryot. Cell 12:1052
    [Google Scholar]
  38. 38. 
    Ferris HU, Coles M, Lupas AN, Hartmann MD 2014. Crystallographic snapshot of the Escherichia coli EnvZ histidine kinase in an active conformation. J. Struct. Biol. 186:376–79
    [Google Scholar]
  39. 39. 
    Ferris HU, Dunin-Horkawicz S, Hornig N, Hulko M, Martin J et al. 2012. Mechanism of regulation of receptor histidine kinases. Structure 20:56–66
    [Google Scholar]
  40. 40. 
    Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J et al. 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–85
    [Google Scholar]
  41. 41. 
    Fodor AA, Aldrich RW. 2004. Influence of conservation on calculations of amino acid covariance in multiple sequence alignments. Proteins 56:211–21
    [Google Scholar]
  42. 42. 
    Galperin MY. 2010. Diversity of structure and function of response regulator output domains. Curr. Opin. Microbiol. 13:150–59
    [Google Scholar]
  43. 43. 
    Gao R, Bouillet S, Stock A 2019. Structural basis of response regulator function. Annu. Rev. Microbiol. 73:175–97
    [Google Scholar]
  44. 44. 
    Gao R, Stock AM. 2009. Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63:133–54
    [Google Scholar]
  45. 45. 
    Gao R, Stock AM. 2010. Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr. Opin. Microbiol. 13:160–67
    [Google Scholar]
  46. 46. 
    Gao R, Stock AM. 2017. Quantitative kinetic analyses of shutting off a two-component system. mBio 8:e00412–17This elegant study shows the (often underestimated) physiologic relevance of histidine-kinase-mediated phosphatase activity in vivo.
    [Google Scholar]
  47. 47. 
    Gardino AK, Villali J, Kivenson A, Lei M, Liu CF et al. 2009. Transient non-native hydrogen bonds promote activation of a signaling protein. Cell 139:1109–18
    [Google Scholar]
  48. 48. 
    Goulian M. 2010. Two-component signaling circuit structure and properties. Curr. Opin. Microbiol. 13:184–89
    [Google Scholar]
  49. 49. 
    Grebe TW, Stock JB. 1999. The histidine protein kinase superfamily. Adv. Microb. Physiol. 41:139–227
    [Google Scholar]
  50. 50. 
    Gushchin I, Gordeliy V. 2018. Transmembrane signal transduction in two-component systems: piston, scissoring, or helical rotation. ? BioEssays 40:1700197
    [Google Scholar]
  51. 51. 
    Gushchin I, Melnikov I, Polovinkin V, Ishchenko A, Yuzhakova A et al. 2017. Mechanism of transmembrane signaling by sensor histidine kinases. Science 356:eaah6345Signal-transduction mechanism of a transmembrane histidine kinase revealed by crystal structures that include the transmembrane portion.
    [Google Scholar]
  52. 52. 
    Gutu AD, Wayne KJ, Sham LT, Winkler ME 2010. Kinetic characterization of the WalRKSpn (VicRK) two-component system of Streptococcus pneumoniae: dependence of WalKSpn (VicK) phosphatase activity on its PAS domain. J. Bacteriol. 192:2346–58
    [Google Scholar]
  53. 53. 
    Hart Y, Alon U. 2013. The utility of paradoxical components in biological circuits. Mol. Cell 49:213–21
    [Google Scholar]
  54. 54. 
    Herschlag D, Jencks WP. 1987. The effect of divalent metal ions on the rate and transition-state structure of phosphoryl-transfer reactions. J. Am. Chem. Soc. 109:4665–74
    [Google Scholar]
  55. 55. 
    Herschlag D, Jencks WP. 1990. Catalysis of the hydrolysis of phosphorylated pyridines by Mg(OH)+: a possible model for enzymic phosphoryl transfer. Biochemistry 29:5172–79
    [Google Scholar]
  56. 56. 
    Huynh TN, Noriega CE, Stewart V 2010. Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX. PNAS 107:21140–45
    [Google Scholar]
  57. 57. 
    Huynh TN, Noriega CE, Stewart V 2013. Missense substitutions reflecting regulatory control of transmitter phosphatase activity in two-component signalling. Mol. Microbiol. 88:459–72
    [Google Scholar]
  58. 58. 
    Huynh TN, Stewart V. 2011. Negative control in two-component signal transduction by transmitter phosphatase activity. Mol. Microbiol. 82:275–86
    [Google Scholar]
  59. 59. 
    Igoshin OA, Alves R, Savageau MA 2008. Hysteretic and graded responses in bacterial two-component signal transduction. Mol. Microbiol. 68:1196–215
    [Google Scholar]
  60. 60. 
    Immormino RM, Silversmith RE, Bourret RB 2016. A variable active site residue influences the kinetics of response regulator phosphorylation and dephosphorylation. Biochemistry 55:5595–609
    [Google Scholar]
  61. 61. 
    Jacob-Dubuisson F, Mechaly A, Betton J-M, Antoine R 2018. Structural insights into the signalling mechanisms of two-component systems. Nat. Rev. Microbiol. 16:585–93
    [Google Scholar]
  62. 62. 
    James LC, Tawfik DS. 2003. Conformational diversity and protein evolution—a 60-year-old hypothesis revisited. Trends Biochem. Sci. 28:361–68
    [Google Scholar]
  63. 63. 
    Janiak-Spens F, Cook PF, West AH 2005. Kinetic analysis of YPD1-dependent phosphotransfer reactions in the yeast osmoregulatory phosphorelay system. Biochemistry 44:377–86
    [Google Scholar]
  64. 64. 
    Jiang P, Ninfa AJ. 1999. Regulation of autophosphorylation of Escherichia coli nitrogen regulator II by the PII signal transduction protein. J. Bacteriol. 181:1906–11
    [Google Scholar]
  65. 65. 
    Jung K, Fried L, Behr S, Heermann R 2012. Histidine kinases and response regulators in networks. Curr. Opin. Microbiol. 15:118–24
    [Google Scholar]
  66. 66. 
    Kee JM, Muir TW. 2012. Chasing phosphohistidine, an elusive sibling in the phosphoamino acid family. ACS Chem. Biol. 7:44–51
    [Google Scholar]
  67. 67. 
    Kou X, Liu Y, Li C, Liu M, Jiang L 2018. Dimerization and conformational exchanges of the receiver domain of response regulator PhoB from Escherichia coli. J. Phys. Chem. B 122:5749–57
    [Google Scholar]
  68. 68. 
    Krell T, Lacal J, Busch A, Silva-Jimenez H, Guazzaroni ME, Ramos JL 2010. Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu. Rev. Microbiol. 64:539–59
    [Google Scholar]
  69. 69. 
    Lad C, Williams NH, Wolfenden R 2003. The rate of hydrolysis of phosphomonoester dianions and the exceptional catalytic proficiencies of protein and inositol phosphatases. PNAS 100:5607–10
    [Google Scholar]
  70. 70. 
    Lan G, Sartori P, Neumann S, Sourjik V, Tu Y 2012. The energy-speed-accuracy tradeoff in sensory adaptation. Nat. Phys. 8:422–28
    [Google Scholar]
  71. 71. 
    Lan G, Tu Y. 2016. Information processing in bacteria: memory, computation, and statistical physics: a key issues review. Rep. Prog. Phys. 79:052601
    [Google Scholar]
  72. 72. 
    Landry BP, Palanki R, Dyulgyarov N, Hartsough LA, Tabor JJ 2018. Phosphatase activity tunes two-component system sensor detection threshold. Nat. Commun. 9:1433
    [Google Scholar]
  73. 73. 
    Lassak J, Bubendorfer S, Thormann KM 2013. Domain analysis of ArcS, the hybrid sensor kinase of the Shewanella oneidensis MR-1 Arc two-component system, reveals functional differentiation of its two receiver domains. J. Bacteriol. 195:482–92
    [Google Scholar]
  74. 74. 
    Lassila JK, Zalatan JG, Herschlag D 2011. Biological phosphoryl-transfer reactions: understanding mechanism and catalysis. Annu. Rev. Biochem. 80:669–702
    [Google Scholar]
  75. 75. 
    Laub MT, Goulian M. 2007. Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41:121–45
    [Google Scholar]
  76. 76. 
    Lesne E, Dupre E, Lensink MF, Locht C, Antoine R, Jacob-Dubuisson F 2018. Coiled-coil antagonism regulates activity of Venus flytrap-domain-containing sensor kinases of the BvgS family. mBio 9:e02052–17
    [Google Scholar]
  77. 77. 
    Liu Y, Rose J, Huang S, Hu Y, Wu Q et al. 2017. A pH-gated conformational switch regulates the phosphatase activity of bifunctional HisKA-family histidine kinases. Nat. Commun. 8:2104
    [Google Scholar]
  78. 78. 
    Lori C, Kaczmarczyk A, de Jong I, Jenal U 2018. A single-domain response regulator functions as an integrating hub to coordinate general stress response and development in alphaproteobacteria. mBio 9:e00809-18. Erratum. 2018. mBio 9:e01534–18
    [Google Scholar]
  79. 79. 
    Lukat GS, Stock AM, Stock JB 1990. Divalent metal ion binding to the CheY protein and its significance to phosphotransfer in bacterial chemotaxis. Biochemistry 29:5436–42
    [Google Scholar]
  80. 80. 
    Lupas AN, Bassler J. 2017. Coiled coils—a model system for the 21st century. Trends Biochem. Sci. 42:130–40
    [Google Scholar]
  81. 81. 
    Marina A, Waldburger CD, Hendrickson WA 2005. Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24:4247–59
    [Google Scholar]
  82. 82. 
    Marsico F, Burastero O, Defelipe LA, Lopez ED, Arrar M et al. 2018. Multiscale approach to the activation and phosphotransfer mechanism of CpxA histidine kinase reveals a tight coupling between conformational and chemical steps. Biochem. Biophys. Res. Commun. 498:305–12
    [Google Scholar]
  83. 83. 
    Mascher T, Helmann JD, Unden G 2006. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70:910–38
    [Google Scholar]
  84. 84. 
    Matsubara M, Mizuno T. 2000. The SixA phospho-histidine phosphatase modulates the ArcB phosphorelay signal transduction in Escherichia coli. FEBS Lett 470:118–24
    [Google Scholar]
  85. 85. 
    Mechaly AE, Sassoon N, Betton JM, Alzari PM 2014. Segmental helical motions and dynamical asymmetry modulate histidine kinase autophosphorylation. PLOS Biol 12:e1001776The first crystal structure of a histidine kinase trapped in autophosphorylation confirms symmetry/asymmetry-related activity switching.
    [Google Scholar]
  86. 86. 
    Mechaly AE, Soto Diaz S, Sassoon N, Buschiazzo A, Betton JM, Alzari PM 2017. Structural coupling between autokinase and phosphotransferase reactions in a bacterial histidine kinase. Structure 25:939–44.e3
    [Google Scholar]
  87. 87. 
    Mika F, Hengge R. 2005. A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of σS (RpoS) in E. coli. Genes Dev 19:2770–81
    [Google Scholar]
  88. 88. 
    Möglich A, Ayers RA, Moffat K 2009. Design and signaling mechanism of light-regulated histidine kinases. J. Mol. Biol. 385:1433–44
    [Google Scholar]
  89. 89. 
    Möglich A, Ayers RA, Moffat K 2010. Addition at the molecular level: signal integration in designed Per–ARNT–Sim receptor proteins. J. Mol. Biol. 400:477–86
    [Google Scholar]
  90. 90. 
    Morcos F, Pagnani A, Lunt B, Bertolino A, Marks DS et al. 2011. Direct-coupling analysis of residue coevolution captures native contacts across many protein families. PNAS 108:E1293–301
    [Google Scholar]
  91. 91. 
    Nakamura H, Kumita H, Imai K, Iizuka T, Shiro Y 2004. ADP reduces the oxygen-binding affinity of a sensory histidine kinase, FixL: the possibility of an enhanced reciprocating kinase reaction. PNAS 101:2742–46
    [Google Scholar]
  92. 92. 
    Noriega CE, Schmidt R, Gray MJ, Chen LL, Stewart V 2008. Autophosphorylation and dephosphorylation by soluble forms of the nitrate-responsive sensors NarX and NarQ from Escherichia coli K-12. J. Bacteriol. 190:3869–76
    [Google Scholar]
  93. 93. 
    Nussinov R, Ma B, Tsai CJ 2014. Multiple conformational selection and induced fit events take place in allosteric propagation. Biophys. Chem. 186:22–30
    [Google Scholar]
  94. 94. 
    Ogino T, Matsubara M, Kato N, Nakamura Y, Mizuno T 1998. An Escherichia coli protein that exhibits phosphohistidine phosphatase activity towards the HPt domain of the ArcB sensor involved in the multistep His-Asp phosphorelay. Mol. Microbiol. 27:573–85
    [Google Scholar]
  95. 95. 
    Page SC, Immormino RM, Miller TH, Bourret RB 2016. Experimental analysis of functional variation within protein families: receiver domain autodephosphorylation kinetics. J. Bacteriol. 198:2483–93
    [Google Scholar]
  96. 96. 
    Parashar V, Mirouze N, Dubnau DA, Neiditch MB 2011. Structural basis of response regulator dephosphorylation by Rap phosphatases. PLOS Biol 9:e1000589
    [Google Scholar]
  97. 97. 
    Pazy Y, Motaleb MA, Guarnieri MT, Charon NW, Zhao R, Silversmith RE 2010. Identical phosphatase mechanisms achieved through distinct modes of binding phosphoprotein substrate. PNAS 107:1924–29
    [Google Scholar]
  98. 98. 
    Pflüger T, Hernandez CF, Lewe P, Frank F, Mertens H et al. 2018. Signaling ammonium across membranes through an ammonium sensor histidine kinase. Nat. Commun. 9:164
    [Google Scholar]
  99. 99. 
    Pickart CM, Jencks WP. 1984. Energetics of the calcium-transporting ATPase. J. Biol. Chem. 259:1629–43
    [Google Scholar]
  100. 100. 
    Plesniak L, Horiuchi Y, Sem D, Meinenger D, Stiles L et al. 2002. Probing the nucleotide binding domain of the osmoregulator EnvZ using fluorescent nucleotide derivatives. Biochemistry 41:13876–82
    [Google Scholar]
  101. 101. 
    Podgornaia AI, Casino P, Marina A, Laub MT 2013. Structural basis of a rationally rewired protein-protein interface critical to bacterial signaling. Structure 21:1636–47
    [Google Scholar]
  102. 102. 
    Podgornaia AI, Laub MT. 2013. Determinants of specificity in two-component signal transduction. Curr. Opin. Microbiol. 16:156–62
    [Google Scholar]
  103. 103. 
    Podgornaia AI, Laub MT. 2015. Protein evolution: pervasive degeneracy and epistasis in a protein-protein interface. Science 347:673–77High tolerance for mutations at HK:RR interfaces, with epistasis, is shown to underlie TCS evolution.
    [Google Scholar]
  104. 104. 
    Pontiggia F, Pachov DV, Clarkson MW, Villali J, Hagan MF et al. 2015. Free energy landscape of activation in a signalling protein at atomic resolution. Nat. Commun. 6:7284
    [Google Scholar]
  105. 105. 
    Porter SL, Wadhams GH, Armitage JP 2011. Signal processing in complex chemotaxis pathways. Nat. Rev. Microbiol. 9:153
    [Google Scholar]
  106. 106. 
    Potter CA, Ward A, Laguri C, Williamson MP, Henderson PJ, Phillips-Jones MK 2002. Expression, purification and characterisation of full-length histidine protein kinase RegB from Rhodobacter sphaeroides. J. Mol. Biol 320:201–13
    [Google Scholar]
  107. 107. 
    Rivera-Cancel G, Ko WH, Tomchick DR, Correa F, Gardner KH 2014. Full-length structure of a monomeric histidine kinase reveals basis for sensory regulation. PNAS 111:17839–44
    [Google Scholar]
  108. 108. 
    Ruder WC, Lu T, Collins JJ 2011. Synthetic biology moving into the clinic. Science 333:1248–52
    [Google Scholar]
  109. 109. 
    Saita E, Abriata LA, Tsai YT, Trajtenberg F, Lemmin T et al. 2015. A coiled coil switch mediates cold sensing by the thermosensory protein DesK. Mol. Microbiol. 98:258–71
    [Google Scholar]
  110. 110. 
    Salazar ME, Laub MT. 2015. Temporal and evolutionary dynamics of two-component signaling pathways. Curr. Opin. Microbiol. 24:7–14
    [Google Scholar]
  111. 111. 
    Schmidt NW, Grigoryan G, DeGrado WF 2017. The accommodation index measures the perturbation associated with insertions and deletions in coiled-coils: application to understand signaling in histidine kinases. Protein Sci 26:414–35
    [Google Scholar]
  112. 112. 
    Schulte JE, Goulian M. 2018. The phosphohistidine phosphatase SixA targets a phosphotransferase system. mBio 9:e01666–18
    [Google Scholar]
  113. 113. 
    Shi L, Liu W, Hulett FM 1999. Decay of activated Bacillus subtilis Pho response regulator, PhoP∼P, involves the PhoR∼P intermediate. Biochemistry 38:10119–25
    [Google Scholar]
  114. 114. 
    Singh M, Berger B, Kim PS, Berger JM, Cochran AG 1998. Computational learning reveals coiled coil-like motifs in histidine kinase linker domains. PNAS 95:2738–43
    [Google Scholar]
  115. 115. 
    Siryaporn A, Goulian M. 2008. Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli. Mol. Microbiol 70:494–506
    [Google Scholar]
  116. 116. 
    Skerker JM, Perchuk BS, Siryaporn A, Lubin EA, Ashenberg O et al. 2008. Rewiring the specificity of two-component signal transduction systems. Cell 133:1043–54This landmark study uncovers molecular bases of the HK:RR specificity code in TCSs.
    [Google Scholar]
  117. 117. 
    Skerker JM, Prasol MS, Perchuk BS, Biondi EG, Laub MT 2005. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLOS Biol 3:e334
    [Google Scholar]
  118. 118. 
    Stewart RC, VanBruggen R, Ellefson DD, Wolfe AJ 1998. TNP-ATP and TNP-ADP as probes of the nucleotide binding site of CheA, the histidine protein kinase in the chemotaxis signal transduction pathway of Escherichia coli. Biochemistry 37:12269–79
    [Google Scholar]
  119. 119. 
    Stewart V, Chen LL. 2010. The S helix mediates signal transmission as a HAMP domain coiled-coil extension in the NarX nitrate sensor from Escherichia coli K-12. J. Bacteriol. 192:734–45
    [Google Scholar]
  120. 120. 
    Stock AM, Robinson VL, Goudreau PN 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183–215
    [Google Scholar]
  121. 121. 
    Stock J, Da Re S 2000. Signal transduction: response regulators on and off. Curr. Biol. 10:R420–24
    [Google Scholar]
  122. 122. 
    Stock JB, Stock AM, Mottonen JM 1990. Signal transduction in bacteria. Nature 344:395–400
    [Google Scholar]
  123. 123. 
    Straube R. 2014. Reciprocal regulation as a source of ultrasensitivity in two-component systems with a bifunctional sensor kinase. PLOS Comput. Biol. 10:e1003614
    [Google Scholar]
  124. 124. 
    Szurmant H, Weigt M. 2017. Inter-residue, inter-protein and inter-family coevolution: bridging the scales. Curr. Opin. Struct. Biol. 50:26–32
    [Google Scholar]
  125. 125. 
    Teran-Melo JL, Pena-Sandoval GR, Silva-Jimenez H, Rodriguez C, Alvarez AF, Georgellis D 2018. Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB. J. Biol. Chem. 293:13214–23
    [Google Scholar]
  126. 126. 
    Tomomori C, Tanaka T, Dutta R, Park H, Saha SK et al. 1999. Solution structure of the homodimeric core domain of Escherichia coli histidine kinase EnvZ. Nat. Struct. Biol. 6:729–34
    [Google Scholar]
  127. 127. 
    Townsend GE 2nd, Raghavan V, Zwir I, Groisman EA 2013. Intramolecular arrangement of sensor and regulator overcomes relaxed specificity in hybrid two-component systems. PNAS 110:E161–69
    [Google Scholar]
  128. 128. 
    Toyoshima C. 2009. How Ca2+-ATPase pumps ions across the sarcoplasmic reticulum membrane. Biochim. Biophys. Acta 1793:941–46
    [Google Scholar]
  129. 129. 
    Trajtenberg F, Albanesi D, Ruetalo N, Botti H, Mechaly AE et al. 2014. Allosteric activation of bacterial response regulators: the role of the cognate histidine kinase beyond phosphorylation. mBio 5:e02105
    [Google Scholar]
  130. 130. 
    Trajtenberg F, Graña M, Ruetalo N, Botti H, Buschiazzo A 2010. Structural and enzymatic insights into the ATP binding and autophosphorylation mechanism of a sensor histidine kinase. J. Biol. Chem. 285:24892–903
    [Google Scholar]
  131. 131. 
    Trajtenberg F, Imelio JA, Machado MR, Larrieux N, Marti MA et al. 2016. Regulation of signaling directionality revealed by 3D snapshots of a kinase:regulator complex in action. eLife 5:e21422Crystal structures of a histidine kinase:regulator complex uncover distinct signaling states and determinants of phosphoryl-transfer directionality.
    [Google Scholar]
  132. 132. 
    Varughese KI, Tsigelny I, Zhao H 2006. The crystal structure of beryllofluoride Spo0F in complex with the phosphotransferase Spo0B represents a phosphotransfer pretransition state. J. Bacteriol. 188:4970–77
    [Google Scholar]
  133. 133. 
    Wang B, Zhao A, Novick RP, Muir TW 2014. Activation and inhibition of the receptor histidine kinase AgrC occurs through opposite helical transduction motions. Mol. Cell 53:929–40
    [Google Scholar]
  134. 134. 
    Wang C, Sang J, Wang J, Su M, Downey JS et al. 2013. Mechanistic insights revealed by the crystal structure of a histidine kinase with signal transducer and sensor domains. PLOS Biol 11:e1001493
    [Google Scholar]
  135. 135. 
    Weigel N, Kukuruzinska MA, Nakazawa A, Waygood EB, Roseman S 1982. Sugar transport by the bacterial phosphotransferase system. Phosphoryl transfer reactions catalyzed by enzyme I of Salmonella typhimurium. J. Biol. Chem 257:14477–91
    [Google Scholar]
  136. 136. 
    Weigt M, White RA, Szurmant H, Hoch JA, Hwa T 2009. Identification of direct residue contacts in protein-protein interaction by message passing. PNAS 106:67–72
    [Google Scholar]
  137. 137. 
    Willett JW, Herrou J, Briegel A, Rotskoff G, Crosson S 2015. Structural asymmetry in a conserved signaling system that regulates division, replication, and virulence of an intracellular pathogen. PNAS 112:E3709–18
    [Google Scholar]
  138. 138. 
    Willett JW, Kirby JR. 2012. Genetic and biochemical dissection of a HisKA domain identifies residues required exclusively for kinase and phosphatase activities. PLOS Genet 8:e1003084
    [Google Scholar]
  139. 139. 
    Wojnowska M, Yan J, Sivalingam Ganesh N, Cryar A, Gor J et al. 2013. Autophosphorylation activity of a soluble hexameric histidine kinase correlates with the shift in protein conformational equilibrium. Chem. Biol. 20:1411–20
    [Google Scholar]
  140. 140. 
    Wolanin PM, Webre DJ, Stock JB 2003. Mechanism of phosphatase activity in the chemotaxis response regulator CheY. Biochemistry 42:14075–82
    [Google Scholar]
  141. 141. 
    Wolfe AJ. 2010. Physiologically relevant small phosphodonors link metabolism to signal transduction. Curr. Opin. Microbiol. 13:204–9
    [Google Scholar]
  142. 142. 
    Wolfenden R, Ridgway C, Young G 1998. Spontaneous hydrolysis of ionized phosphate monoesters and diesters and the proficiencies of phosphatases and phosphodiesterases as catalysts. J. Am. Chem. Soc. 120:833–34
    [Google Scholar]
  143. 143. 
    Wuichet K, Cantwell BJ, Zhulin IB 2010. Evolution and phyletic distribution of two-component signal transduction systems. Curr. Opin. Microbiol. 13:219–25
    [Google Scholar]
  144. 144. 
    Xie Q, Zhao A, Jeffrey PD, Kim MK, Bassler BL et al. 2019. Identification of a molecular latch that regulates staphylococcal virulence. Cell Chem. Biol. 26:4548–58.e4AgrC further confirms universal mechanisms of S-helix rearrangements linked to modulation of the ABD-DHp interaction.
    [Google Scholar]
  145. 145. 
    Xu Q, Porter SW, West AH 2003. The Yeast YPD1/SLN1 complex. Structure 11:1569–81
    [Google Scholar]
  146. 146. 
    Yamada S, Sugimoto H, Kobayashi M, Ohno A, Nakamura H, Shiro Y 2009. Structure of PAS-linked histidine kinase and the response regulator complex. Structure 17:1333–44
    [Google Scholar]
  147. 147. 
    Yeo WS, Zwir I, Huang HV, Shin D, Kato A, Groisman EA 2012. Intrinsic negative feedback governs activation surge in two-component regulatory systems. Mol. Cell 45:409–21
    [Google Scholar]
  148. 148. 
    Zapf J, Sen U, Madhusudan Hoch JA, Varughese KI 2000. A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 8:851–62
    [Google Scholar]
  149. 149. 
    Zhao R, Collins EJ, Bourret RB, Silversmith RE 2002. Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat. Struct. Biol. 9:570–75
    [Google Scholar]
  150. 150. 
    Zhao X, Copeland DM, Soares AS, West AH 2008. Crystal structure of a complex between the phosphorelay protein YPD1 and the response regulator domain of SLN1 bound to a phosphoryl analog. J. Mol. Biol. 375:1141–51
    [Google Scholar]
  151. 151. 
    Zschiedrich CP, Keidel V, Szurmant H 2016. Molecular mechanisms of two-component signal transduction. J. Mol. Biol. 428:3752–75
    [Google Scholar]
/content/journals/10.1146/annurev-micro-091018-054627
Loading
/content/journals/10.1146/annurev-micro-091018-054627
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error