Signal Transduction in Histidine Kinases: Insights from New Structures

Structure

Volumn 23, Issue 6, 2015, Pages 981-994

  Bhate, ManasiA P ^a   Molnar, KathleenA S ^a,b   Goulian, Mark ^b   Degrado, William F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; PROTEIN HISTIDINE KINASE; PROTEIN KINASE;

ASYMMETRIC CATALYSIS; CRYSTAL STRUCTURE; ENZYMOLOGY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; THERMODYNAMICS; AMINO ACID SEQUENCE; CATALYSIS; CHEMISTRY; DIMERIZATION; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PHYSIOLOGY;

BACTERIA (MICROORGANISMS);

AMINO ACID SEQUENCE; CATALYSIS; DIMERIZATION; HISTIDINE KINASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN KINASES; SIGNAL TRANSDUCTION; THERMODYNAMICS;

EID: 84930376521     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.04.002     Document Type: Review

References (83)

1. P.S. Aguilar, A.M. Hernandez-Arriaga, L.E. Cybulski, A.C. Erazo, and D. de Mendoza Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis EMBO J. 20 2001 1681 1691
2. M.V. Airola, K.J. Watts, A.M. Bilwes, and B.R. Crane Structure of concatenated HAMP domains provides a mechanism for signal transduction Structure 18 2010 436 448
3. D. Albanesi, M. Martín, F. Trajtenberg, M.C. Mansilla, A. Haouz, P.M. Alzari, D. de Mendoza, and A. Buschiazzo Structural plasticity and catalysis regulation of a thermosensor histidine kinase Proc. Natl. Acad. Sci. USA 106 2009 16185 16190
4. P. Ames, Q. Zhou, and J.S. Parkinson Mutational analysis of the connector segment in the HAMP domain of Tsr, the Escherichia coli serine chemoreceptor J.A Bacteriol. 190 2008 6676 6685
5. J.A. Appleman, L.-L. Chen, and V. Stewart Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases J.A Bacteriol. 185 2003 4872 4882
6. O. Ashenberg, A.E. Keating, and M.T. Laub Helix bundle loops determine whether histidine kinases autophosphorylate in cis or in trans J.A Mol. Biol. 425 2013 1198 1209
7. M.W. Bader, S. Sanowar, M.E. Daley, A.R. Schneider, U. Cho, W. Xu, R.E. Klevit, H. Le Moual, and S.I. Miller Recognition of antimicrobial peptides by a bacterial sensor kinase Cell 122 2005 461 472
8. R.B. Bourret Receiver domain structure and function in response regulator proteins Curr. Opin. Microbiol. 13 2010 142 149
9. R.B. Bourret, S.A. Thomas, S.C. Page, R.L. Creager-Allen, A.M. Moore, and R.E. Silversmith Measurement of response regulator autodephosphorylation rates spanning six orders of magnitude Methods Enzymol. 471 2010 89 114
10. M.H. Buckstein, J. He, and H. Rubin Characterization of nucleotide pools as a function of physiological state in Escherichia coli J.A Bacteriol. 190 2008 718 726
11. E.J. Capra, and M.T. Laub Evolution of two-component signal transduction systems Annu. Rev. Microbiol. 66 2012 325 347
12. P. Casino, V. Rubio, and A. Marina Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction Cell 139 2009 325 336
13. P. Casino, V. Rubio, and A. Marina The mechanism of signal transduction by two-component systems Curr. Opin. Struct. Biol. 20 2010 763 771
14. P. Casino, L. Miguel-Romero, and A. Marina Visualizing autophosphorylation in histidine kinases Nat. Commun. 5 2014 3258
15. C. Chang, C. Tesar, M. Gu, G. Babnigg, A. Joachimiak, P. Raj Pokkuluri, H. Szurmant, and M. Schiffer Extracytoplasmic PAS-like domains are common in signal transduction proteins J.A Bacteriol. 192 2010 1156 1159
16. S.A. Chervitz, and J.J. Falke Molecular mechanism of transmembrane signaling by the aspartate receptor: a model Proc. Natl. Acad. Sci. USA 93 1996 2545 2550
17. J. Cheung, and W.A. Hendrickson Structural analysis of ligand stimulation of the histidine kinase NarX Structure 17 2009 190 201
18. J. Cheung, and W.A. Hendrickson Sensor domains of two-component regulatory systems Curr. Opin. Microbiol. 13 2010 116 123
19. J. Cheung, C.A. Bingman, M. Reyngold, W.A. Hendrickson, and C.D. Waldburger Crystal structure of a functional dimer of the PhoQ sensor domain J.A Biol. Chem. 283 2008 13762 13770
20. R.P. Diensthuber, M. Bommer, T. Gleichmann, and A. Möglich Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators Structure 21 2013 1127 1136
21. J.J. Falke, and A.H. Erbse The piston rises again Structure 17 2009 1149 1151
22. H.U. Ferris, S. Dunin-Horkawicz, L.G. Mondéjar, M. Hulko, K. Hantke, J. Martin, J.E. Schultz, K. Zeth, A.N. Lupas, and M. Coles The mechanisms of HAMP-mediated signaling in transmembrane receptors Structure 19 2011 378 385
23. H.U. Ferris, S. Dunin-Horkawicz, N. Hornig, M. Hulko, J. Martin, J.E. Schultz, K. Zeth, A.N. Lupas, and M. Coles Mechanism of regulation of receptor histidine kinases Structure 20 2012 56 66
24. H.U. Ferris, M. Coles, A.N. Lupas, and M.D. Hartmann Crystallographic snapshot of the Escherichia coli EnvZ histidine kinase in an active conformation J.A Struct. Biol. 186 2014 1 4
25. S.L. Fisher, S.K. Kim, B.L. Wanner, and C.T. Walsh Kinetic comparison of the specificity of the vancomycin resistance VanS for two response regulators, VanR and PhoB Biochemistry 35 1996 4732 4740
26. R. Gao, and A.M. Stock Biological insights from structures of two-component proteins Annu. Rev. Microbiol. 63 2009 133 154
27. S.D. Goldberg, G.D. Clinthorne, M. Goulian, and W.F. DeGrado Transmembrane polar interactions are required for signaling in the Escherichia coli sensor kinase PhoQ Proc. Natl. Acad. Sci. USA 107 2010 8141 8146
28. + channels, and integrin receptors Annu. Rev. Biochem. 80 2011 211 237
29. E.A. Groisman The pleiotropic two-component regulatory system PhoP-PhoQ J.A Bacteriol. 183 2001 1835
30. A.D. Gutu, K.J. Wayne, L.-T. Sham, and M.E. Winkler Kinetic characterization of the WalRKSpn (VicRK) two-component system of Streptococcus pneumoniae: dependence of WalKSpn (VicK) phosphatase activity on its PAS domain J.A Bacteriol. 192 2010 2346 2358
31. G.L. Hazelbauer, J.J. Falke, and J.S. Parkinson Bacterial chemoreceptors: high-performance signaling in networked arrays Trends Biochem. Sci. 33 2008 9 19
32. J.T. Henry, and S. Crosson Ligand-binding PAS domains in a genomic, cellular, and structural context Annu. Rev. Microbiol. 65 2011 261 286
33. X. Hu, J. Zhao, W.F. Degrado, and A.N. Binns Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals Proc. Natl. Acad. Sci. USA 110 2013 678 683
34. M. Hulko, F. Berndt, M. Gruber, J.U. Linder, V. Truffault, A. Schultz, J. Martin, J.E. Schultz, A.N. Lupas, and M. Coles The HAMP domain structure implies helix rotation in transmembrane signaling Cell 126 2006 929 940
35. M.M. Igo, A.J. Ninfa, J.B. Stock, and T.J. Silhavy Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor Genes Dev. 3 1989 1725 1734
36. P. Jiang, J.A. Peliska, and A.J. Ninfa Asymmetry in the autophosphorylation of the two-component regulatory system transmitter protein nitrogen regulator II of Escherichia coli Biochemistry 39 2000 5057 5065
37. K. Jung, L. Fried, S. Behr, and R. Heermann Histidine kinases and response regulators in networks Curr. Opin. Microbiol. 15 2012 118 124
38. S. Kaspar, R. Perozzo, S. Reinelt, M. Meyer, K. Pfister, L. Scapozza, and M. Bott The periplasmic domain of the histidine autokinase CitA functions as a highly specific citrate receptor Mol. Microbiol. 33 1999 858 872
39. D. Kim, and S. Forst Genomic analysis of the histidine kinase family in bacteria and archaea Microbiology 147 2001 1197 1212
40. J. Kuriyan, and D. Eisenberg The origin of protein interactions and allostery in colocalization Nature 450 2007 983 990
41. M.T. Laub, and M. Goulian Specificity in two-component signal transduction pathways Annu. Rev. Genet. 41 2007 121 145
42. D.J. Leahy The ins and outs of EGFR asymmetry Cell 142 2010 513 515
43. T. Lemmin, C.S. Soto, G. Clinthorne, W.F. DeGrado, and M. Dal Peraro Assembly of the transmembrane domain of E.A coli PhoQ histidine kinase: implications for signal transduction from molecular simulations PLoS Comput. Biol. 9 2013 e1002878
44. M. Li, and G.L. Hazelbauer Selective allosteric coupling in core chemotaxis signaling complexes Proc. Natl. Acad. Sci. USA 111 2014 1 6
45. G.-W. Li, D. Burkhardt, C. Gross, and J.S. Weissman Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources Cell 157 2014 624 635
46. Y.-H. Lin, B.D. Pierce, F. Fang, A. Wise, A.N. Binns, and D.G. Lynn Role of the VirA histidine autokinase of Agrobacterium tumefaciens in the initial steps of pathogenesis Front. Plant Sci. 5 2014 195
47. E.C. Lowe, A. Baslé, M. Czjzek, S.J. Firbank, and D.N. Bolam A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system Proc. Natl. Acad. Sci. USA 109 2012 7298 7303
48. A. Marina, C.D. Waldburger, and W.A. Hendrickson Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein EMBO J. 24 2005 4247 4259
49. T. Mascher Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria FEMS Microbiol. Lett. 264 2006 133 144
50. T. Mascher, J.D. Helmann, and G. Unden Stimulus perception in bacterial signal-transducing histidine kinases Microbiol. Mol. Biol. Rev. 70 2006 910 938
51. I. Maslennikov, C. Klammt, E. Hwang, G. Kefala, M. Okamura, and L. Esquivies Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis Proc. Natl. Acad. Sci. USA 107 2010 10902 10907
52. V.R.F. Matias, and T.J. Beveridge Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus J.A Bacteriol. 188 2006 1011 1021
53. A.E. Mechaly, N. Sassoon, J.-M. Betton, and P.M. Alzari Segmental helical motions and dynamical asymmetry modulate histidine kinase autophosphorylation PLoS Biol. 12 2014 e1001776
54. M.V. Milburn, G.G. Prive, D.L. Milligan, W.G. Scott, J. Yeh, J. Jancarik, D.E. Koshland Jr., and S.-H. Kim Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor Science 254 1991 1342 1346
55. S.I. Miller, A.M. Kukral, and J.J. Mekalanos A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence Proc. Natl. Acad. Sci. USA 86 1989 5054 5058
56. A. Möglich, R.A. Ayers, and K. Moffat Design and signaling mechanism of light-regulated histidine kinases J.A Mol. Biol. 385 2009 1433 1444
57. A. Möglich, R.A. Ayers, and K. Moffat Structure and signaling mechanism of Per-ARNT-Sim domains Structure 17 2009 1282 1294
58. K.S. Molnar, M. Bonomi, R. Pellarin, G.D. Clinthorne, G. Gonzalez, S.D. Goldberg, M. Goulian, A. Sali, and W.F. DeGrado Cys-scanning disulfide crosslinking and bayesian modeling probe the transmembrane signaling mechanism of the histidine kinase, PhoQ Structure 22 2014 1239 1251
59. J.O. Moore, and W.A. Hendrickson An asymmetry-to-symmetry switch in signal transmission by the histidine kinase receptor for TMAO Structure 20 2012 729 741
60. R. Moukhametzianov, J.P. Klare, R. Efremov, C. Baeken, A. Göppner, J. Labahn, M. Engelhard, G. Büldt, and V.I. Gordeliy Development of the signal in sensory rhodopsin and its transfer to the cognate transducer Nature 440 2006 115 119
61. M.B. Neiditch, M.J. Federle, A.J. Pompeani, R.C. Kelly, D.L. Swem, P.D. Jeffrey, B.L. Bassler, and F.M. Hughson Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing Cell 126 2006 1095 1108
62. J.S. Parkinson Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases Annu. Rev. Microbiol. 64 2010 101 122
63. A.I. Podgornaia, P. Casino, A. Marina, and M.T. Laub Structural basis of a rationally rewired protein-protein interface critical to bacterial signaling Structure 21 2013 1636 1647
64. R.S. Rabin, and V. Stewart Either of two functionally redundant sensor proteins, NarX and NarQ, is sufficient for nitrate regulation in Escherichia coli K-12 Proc. Natl. Acad. Sci. USA 89 1992 8419 8423
65. D. Russo, and J. Silhavy EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes medium J.A Mol. Biol. 222 1991 567 580
66. J. Schultz, and J. Natarajan Regulated unfolding: a basic principle of intraprotein signalling in modular proteins. Trends in Biochem Sci. 38 2013 538 545
67. M. Sevvana, V. Vijayan, M. Zweckstetter, S. Reinelt, D.R. Madden, R. Herbst-Irmer, G.M. Sheldrick, M. Bott, C. Griesinger, and S. Becker A ligand-induced switch in the periplasmic domain of sensor histidine kinase CitA J.A Mol. Biol. 377 2008 512 523
68. V. Stewart The HAMP signal-conversion domain: static two-state or dynamic three-state? Mol. Microbiol. 91 2014 853 857
69. V. Stewart, and L.-L. Chen The S helix mediates signal transmission as a HAMP domain coiled-coil extension in the NarX nitrate sensor from Escherichia coli K-12 J.A Bacteriol. 192 2010 734 745
70. M. Stock, V.L. Robinson, and P.N. Goudreau Two-component signal transduction Annu. Rev. Biochem. 69 2000 183 215
71. K.E. Swain, and J.J. Falke Structure of the conserved HAMP domain in an intact, membrane-bound chemoreceptor: a disulfide mapping study Biochemistry 46 2007 13684 13695
72. K.E. Swain, M.A. Gonzalez, and J.J. Falke 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
73. T. Tanaka, S. Saha, C. Tomomori, R. Ishima, D. Liu, K.I. Tong, H. Park, R. Dutta, L. Qin, and M. Swindells NMR structure of the histidine kinase domain of E.A coli osmosensor EnvZ Nat. Biotechnol. 396 1998 88 92
74. I. Tews, F. Findeisen, I. Sinning, A. Schultz, J.E. Schultz, and J.U. Linder The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme Science 308 2005 1020 1023
75. F. Trajtenberg, M. Graña, N. Ruétalo, H. Botti, and A. Buschiazzo Structural and enzymatic insights into the ATP binding and autophosphorylation mechanism of a sensor histidine kinase J.A Biol. Chem. 285 2010 24892 24903
76. L.E. Ulrich, and I.B. Zhulin The MiST2 database: a comprehensive genomics resource on microbial signal transduction Nucleic Acids Res. 38 2010 D401 D407
77. R. Utsumi, R.E. Brissette, A. Rampersaud, S.A. Forst, K. Oosawa, and M. Inouye Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate Science 245 1989 1246 1249
78. 2+ as an extracellular signal: environmental regulation of salmonella virulence Cell 84 1996 165 174
79. C. Wang, J. Sang, J. Wang, M. Su, J.S. Downey, Q. Wu, S. Wang, Y. Cai, X. Xu, and J. Wu Mechanistic insights revealed by the crystal structure of a histidine kinase with signal transducer and sensor domains PLoS Biol. 11 2013 e1001493
80. K. Winkler, A. Schultz, and J.E. Schultz The S-helix determines the signal in a Tsr receptor/adenylyl cyclase reporter J.A Biol. Chem. 287 2012 15479 15488
81. W.-S. Yeo, I. Zwir, H.V. Huang, D. Shin, A. Kato, and E.A. Groisman Intrinsic negative feedback governs activation surge in two-component regulatory systems Mol. Cell 45 2012 409 421
82. E.W. Yu, and D.E. Koshland Propagating conformational changes over long (and short) distances in proteins Proc. Natl. Acad. Sci. USA 98 2001 9517 9520
83. Y.-F. Zhou, B. Nan, J. Nan, Q. Ma, S. Panjikar, Y.-H. Liang, Y. Wang, and X.-D. Su C4-dicarboxylates sensing mechanism revealed by the crystal structures of DctB sensor domain J.A Mol. Biol. 383 2008 49 61