Snapshots of Conformational Changes Shed Light into the NtrX Receiver Domain Signal Transduction Mechanism

Journal of Molecular Biology

Volumn 427, Issue 20, 2015, Pages 3258-3272

  Fernández, Ignacio ^a   Otero, Lisandro H ^a,b   Klinke, Sebastián ^a,b   Carrica, Mariela Del Carmen ^a   Goldbaum, Fernando A ^a,b  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b Plataforma Argentina de Biologia Estructural y Metabolomica PLABEM   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DIMER; MONOMER; MUTANT PROTEIN; PROTEIN NTRX; UNCLASSIFIED DRUG; OXYGEN; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE;

ALPHA HELIX; ARTICLE; AUTOPHOSPHORYLATION; BETA SHEET; BIOCHEMICAL ANALYSIS; BRUCELLA ABORTUS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIMERIZATION; ENZYME ACTIVITY; FLUORESCENCE SPECTROSCOPY; HALF LIFE TIME; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SIZE EXCLUSION CHROMATOGRAPHY; WILD TYPE; CELL HYPOXIA; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BRUCELLA ABORTUS; CELL HYPOXIA; CRYSTALLOGRAPHY, X-RAY; OXYGEN; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84942366321     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.06.010     Document Type: Article

References (58)

1. A.M. Stock, V.L. Robinson, and P.N. Goudreau Two-component signal transduction Annu Rev Biochem 69 2000 183 215
2. R. Gao, and A.M. Stock Biological insights from structures of two-component proteins Annu Rev Microbiol 63 2009 133 154
3. G.S. Lukat, W.R. McCleary, A.M. Stock, and J.B. Stock Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors Proc Natl Acad Sci U S A 89 1992 718 722
4. R.E. Silversmith, J.L. Appleby, and R.B. Bourret Catalytic mechanism of phosphorylation and dephosphorylation of CheY: kinetic characterization of imidazole phosphates as phosphodonors and the role of acid catalysis Biochemistry 36 1997 14965 14974
5. S.S. Da Re, D. Deville-Bonne, T. Tolstykh, M. V. r., and J.B. Stock Kinetics of CheY phosphorylation by small molecule phosphodonors FEBS Lett 457 1999 323 326
6. D. Yan, H.S. Cho, C.A. Hastings, M.M. Igo, S.Y. Lee, J.G. Pelton, and et al. Beryllofluoride mimics phosphorylation of NtrC and other bacterial response regulators Proc Natl Acad Sci U S A 96 1999 14789 14794
7. M.J. Corbel Brucellosis: an overview Emerg Infect Dis 3 1997 213 221
8. S. Kohler, V. Foulongne, S. Ouahrani-Bettache, G. Bourg, J. Teyssier, M. Ramuz, and et al. The analysis of the intramacrophagic virulome of Brucella suis deciphers the environment encountered by the pathogen inside the macrophage host cell Proc Natl Acad Sci U S A 99 2002 15711 15716
9. J. Ariza, C. Pigrau, C. Canas, A. Marron, F. Martinez, B. Almirante, and et al. Current understanding and management of chronic hepatosplenic suppurative brucellosis Clin Infect Dis 32 2001 1024 1033
10. D. Colmenero Jde, M.I. Queipo-Ortuno, J. Maria Reguera, M. Angel Suarez-Munoz, S. Martin-Carballino, and P. Morata Chronic hepatosplenic abscesses in Brucellosis. Clinico-therapeutic features and molecular diagnostic approach Diagn Microbiol Infect Dis 42 2002 159 167
11. C. Carrica Mdel, I. Fernandez, M.A. Marti, G. Paris, and F.A. Goldbaum The NtrY/X two-component system of Brucella spp. acts as a redox sensor and regulates the expression of nitrogen respiration enzymes Mol Microbiol 85 2012 39 50
12. C. Carrica Mdel, I. Fernandez, R. Sieira, G. Paris, and F.A. Goldbaum The two-component systems PrrBA and NtrYX co-ordinately regulate the adaptation of Brucella abortus to an oxygen-limited environment Mol Microbiol 88 2013 222 233
13. K. Pawlowski, U. Klosse, and F.J. de Bruijn Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism Mol Gen Genet 231 1991 124 138
14. Y. Kumagai, Z. Cheng, M. Lin, and Y. Rikihisa Biochemical activities of three pairs of Ehrlichia chaffeensis two-component regulatory system proteins involved in inhibition of lysosomal fusion Infect Immun 74 2006 5014 5022
15. J.M. Atack, Y.N. Srikhanta, K.Y. Djoko, J.P. Welch, N.H. Hasri, C.T. Steichen, and et al. Characterization of an ntrX mutant of Neisseria gonorrhoeae reveals a response regulator that controls expression of respiratory enzymes in oxidase-positive proteobacteria J Bacteriol 195 2013 2632 2641
16. D. Wang, H. Xue, Y. Wang, R. Yin, F. Xie, and L. Luo The Sinorhizobium meliloti ntrX gene is involved in succinoglycan production, motility, and symbiotic nodulation on alfalfa Appl Environ Microbiol 79 2013 7150 7159
17. J.M. Skerker, M.S. Prasol, B.S. Perchuk, E.G. Biondi, and M.T. Laub Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis PLoS Biol 3 2005 e334
18. M. Bush, and R. Dixon The role of bacterial enhancer binding proteins as specialized activators of sigma54-dependent transcription Microbiol Mol Biol Rev 76 2012 497 529
19. W.C. Bowman, and R.G. Kranz A bacterial ATP-dependent, enhancer binding protein that activates the housekeeping RNA polymerase Genes Dev 12 1998 1884 1893
20. W. Dischert, P.M. Vignais, and A. Colbeau The synthesis of Rhodobacter capsulatus HupSL hydrogenase is regulated by the two-component HupT/HupR system Mol Microbiol 34 1999 995 1006
21. Z. Cheng, M. Lin, and Y. Rikihisa Ehrlichia chaffeensis proliferation begins with NtrY/NtrX and PutA/GlnA upregulation and CtrA degradation induced by proline and glutamine uptake MBio 5 2014 e02141
22. K.M. Davies, E.D. Lowe, C. Venien-Bryan, and L.N. Johnson The HupR receiver domain crystal structure in its nonphospho and inhibitory phospho states J Mol Biol 385 2009 51 64
23. M.G. Meyer, S. Park, L. Zeringue, M. Staley, M. McKinstry, R.I. Kaufman, and et al. A dimeric two-component receiver domain inhibits the sigma54-dependent ATPase in DctD FASEB J 15 2001 1326 1328
24. M. Doucleff, B. Chen, A.E. Maris, D.E. Wemmer, E. Kondrashkina, and B.T. Nixon Negative regulation of AAA + ATPase assembly by two component receiver domains: a transcription activation mechanism that is conserved in mesophilic and extremely hyperthermophilic bacteria J Mol Biol 353 2005 242 255
25. R.B. Bourret Receiver domain structure and function in response regulator proteins Curr Opin Microbiol 13 2010 142 149
26. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J Mol Biol 372 2007 774 797
27. A. Toro-Roman, T.R. Mack, and A.M. Stock Structural analysis and solution studies of the activated regulatory domain of the response regulator ArcA: a symmetric dimer mediated by the alpha4-beta5-alpha5 face J Mol Biol 349 2005 11 26
28. P. Bachhawat, G.V. Swapna, G.T. Montelione, and A.M. Stock Mechanism of activation for transcription factor PhoB suggested by different modes of dimerization in the inactive and active states Structure 13 2005 1353 1363
29. M. Simonovic, and K. Volz A distinct meta-active conformation in the 1.1-Å resolution structure of wild-type ApoCheY J Biol Chem 276 2001 28637 28640
30. F. Trajtenberg, D. Albanesi, N. Ruetalo, H. Botti, A.E. Mechaly, M. Nieves, and et al. Allosteric activation of bacterial response regulators: the role of the cognate histidine kinase beyond phosphorylation MBio 5 2014 e02105
31. B.E. Scharf Summary of useful methods for two-component system research Curr Opin Microbiol 13 2010 246 252
32. R.L. Creager-Allen, R.E. Silversmith, and R.B. Bourret A link between dimerization and autophosphorylation of the response regulator PhoB J Biol Chem 288 2013 21755 21769
33. S.A. Thomas, R.M. Immormino, R.B. Bourret, and R.E. Silversmith Nonconserved active site residues modulate CheY autophosphorylation kinetics and phosphodonor preference Biochemistry 52 2013 2262 2273
34. S.A. Thomas, J.A. Brewster, and R.B. Bourret Two variable active site residues modulate response regulator phosphoryl group stability Mol Microbiol 69 2008 453 465
35. M. Weinstein, A.F. Lois, G.S. Ditta, and D.R. Helinski Mutants of the two-component regulatory protein FixJ of Rhizobium meliloti that have increased activity at the nifA promoter Gene 134 1993 145 152
36. B.F. Volkman, D. Lipson, D.E. Wemmer, and D. Kern Two-state allosteric behavior in a single-domain signaling protein Science 291 2001 2429 2433
37. C.M. Dyer, and F.W. Dahlquist Switched or not?: the structure of unphosphorylated CheY bound to the N terminus of FliM J Bacteriol 188 2006 7354 7363
38. J. Guhaniyogi, V.L. Robinson, and A.M. Stock Crystal structures of beryllium fluoride-free and beryllium fluoride-bound CheY in complex with the conserved C-terminal peptide of CheZ reveal dual binding modes specific to CheY conformation J Mol Biol 359 2006 624 645
39. L.R. McDonald, J.A. Boyer, and A.L. Lee Segmental motions, not a two-state concerted switch, underlie allostery in CheY Structure 20 2012 1363 1373
40. C.A. Hastings, S.Y. Lee, H.S. Cho, D. Yan, S. Kustu, and D.E. Wemmer High-resolution solution structure of the beryllofluoride-activated NtrC receiver domain Biochemistry 42 2003 9081 9090
41. M.H. Knaggs, F.R. Salsbury, M.H. Edgell, and J.S. Fetrow Insights into correlated motions and long-range interactions in CheY derived from molecular dynamics simulations Biophys J 92 2007 2062 2079
42. A.K. Gardino, J. Villali, A. Kivenson, M. Lei, C.F. Liu, P. Steindel, and et al. Transient non-native hydrogen bonds promote activation of a signaling protein Cell 139 2009 1109 1118
43. J.D. Batchelor, M. Doucleff, C.J. Lee, K. Matsubara, S. De Carlo, J. Heideker, and et al. Structure and regulatory mechanism of Aquifex aeolicus NtrC4: variability and evolution in bacterial transcriptional regulation J Mol Biol 384 2008 1058 1075
44. W. Kabsch Xds Acta Crystallogr D Biol Crystallogr 66 2010 125 132
45. R.M. Keegan, and M.D. Winn Automated search-model discovery and preparation for structure solution by molecular replacement Acta Crystallogr D Biol Crystallogr 63 2007 447 457
46. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, and et al. Overview of the CCP4 suite and current developments Acta Crystallogr D Biol Crystallogr 67 2011 235 242
47. 2 + and BeF3- selects between alternate dimeric states of the receiver domain FASEB J 16 2002 1964 1966
48. G. Bunkoczi, and R.J. Read Improvement of molecular-replacement models with Sculptor Acta Crystallogr D Biol Crystallogr 67 2011 303 312
49. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J Appl Crystallogr 40 2007 658 674
50. K. Cowtan The Buccaneer software for automated model building. 1. Tracing protein chains Acta Crystallogr D Biol Crystallogr 62 2006 1002 1011
51. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr D Biol Crystallogr 66 2010 486 501
52. G. Bricogne, E. Blanc, M. Brandl, C. Flensburg, P. Keller, W. Paciorek, P. Roversi, A. Sharff, O.S. Smart, C. Vonrhein, and T.O. Womack BUSTER version 2.10.1 2014 Global Phasing Ltd Cambridege, United Kingdom
53. V.B. Chen, W.B. Arendall, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, and et al. MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr D Biol Crystallogr 66 2010 12 21
54. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr D Biol Crystallogr 60 2004 2256 2268
55. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, and et al. Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
56. K. Arnold, L. Bordoli, J. Kopp, and T. Schwede The SWISS-MODEL workspace: a Web-based environment for protein structure homology modelling Bioinformatics 22 2006 195 201
57. M. Biasini, S. Bienert, A. Waterhouse, K. Arnold, G. Studer, T. Schmidt, and et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Nucleic Acids Res 42 2014 W252 W258
58. F. Kiefer, K. Arnold, M. Kunzli, L. Bordoli, and T. Schwede The SWISS-MODEL repository and associated resources Nucleic Acids Res 37 2009 D387 D392