Atypical response regulator ChxR from Chlamydia trachomatis is structurally poised for DNA binding

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Barta, Michael L ^a   Hickey, John M ^a   Anbanandam, Asokan ^a   Dyer, Kevin ^b   Hammel, Michal ^b   Hefty, P Scott ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEOTIDE; PROTEIN CHXR; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; CHLAMYDIA TRACHOMATIS; CONFORMATION; DNA BINDING; GEL MOBILITY SHIFT ASSAY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; SMALL ANGLE SCATTERING; TANDEM REPEAT; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; THERMODYNAMICS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHLAMYDIA TRACHOMATIS; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TANDEM REPEAT SEQUENCES; THERMODYNAMICS;

EID: 84898603182     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091760     Document Type: Article

References (80)

1. Gao R, Stock AM (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63: 133-154.
2. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215.
3. Martinez-Hackert E, Stock AM (1997) The DNA-binding domain of OmpR: crystal structures of a winged helix transcription factor. Structure 5: 109-124. (Pubitemid 27102862)
4. Kenney LJ (2002) Structure/function relationships in OmpR and other winged-helix transcription factors. Curr Opin Microbiol 5: 135-141.
5. Barbieri CM, Mack TR, Robinson VL, Miller MT, Stock AM (2010) Regulation of response regulator autophosphorylation through interdomain contacts. J Biol Chem 285: 32325-32335.
6. Friedland N, Mack TR, Yu M, Hung LW, Terwilliger TC, et al. (2007) Domain orientation in the inactive response regulator Mycobacterium tuberculosis MtrA provides a barrier to activation. Biochemistry 46: 6733-6743. (Pubitemid 46906404)
7. Nowak E, Panjikar S, Konarev P, Svergun DI, Tucker PA (2006) The structural basis of signal transduction for the response regulator PrrA from Mycobacterium tuberculosis. J Biol Chem 281: 9659-9666. (Pubitemid 43864684)
8. Robinson VL, Wu T, Stock AM (2003) Structural analysis of the domain interface in DrrB, a response regulator of the OmpR/PhoB subfamily. J Bacteriol 185: 4186-4194. (Pubitemid 36835258)
9. King-Scott J, Nowak E, Mylonas E, Panjikar S, Roessle M, et al. (2007) The structure of a full-length response regulator from Mycobacterium tuberculosis in a stabilized three-dimensional domain-swapped, activated state. J Biol Chem 282: 37717-37729.
10. Menon S, Wang S (2011) Structure of the response regulator PhoP from Mycobacterium tuberculosis reveals a dimer through the receiver domain. Biochemistry 50: 5948-5957.
11. Buckler DR, Zhou Y, Stock AM (2002) Evidence of intradomain and interdomain flexibility in an OmpR/PhoB homolog from Thermotoga maritima. Structure 10: 153-164. (Pubitemid 34164594)
12. Hong E, Lee HM, Ko H, Kim DU, Jeon BY, et al. (2007) Structure of an atypical orphan response regulator protein supports a new phosphorylation- independent regulatory mechanism. J Biol Chem 282: 20667-20675. (Pubitemid 47099998)
13. Hickey JM, Lovell S, Battaile KP, Hu L, Middaugh CR, et al. (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: 32606-32616.
14. Ruiz D, Salinas P, Lopez-Redondo ML, Cayuela ML, Marina A, et al. (2008) Phosphorylation-independent activation of the atypical response regulator NblR. Microbiology 154: 3002-3015.
15. Koo IC, Walthers D, Hefty PS, Kenney LJ, Stephens RS (2006) ChxR is a transcriptional activator in Chlamydia. Proc Natl Acad Sci U S A 103: 750-755. (Pubitemid 43153097)
16. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, et al. (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754-759. (Pubitemid 28489390)
17. Hickey JM, Weldon L, Hefty PS (2011) The atypical OmpR/PhoB response regulator ChxR from Chlamydia trachomatis forms homodimers in vivo and binds a direct repeat of nucleotide sequences. J Bacteriol 193: 389-398.
18. Hickey JM, Hefty PS, Lamb AL (2009) Expression, purification, crystallization and preliminary X-ray analysis of the DNA-binding domain of a Chlamydia trachomatis OmpR/PhoB-subfamily response regulator homolog, ChxR. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 791-794.
19. Marley J, Lu M, Bracken C (2001) A method for efficient isotopic labeling of recombinant proteins. J Biomol NMR 20: 71-75. (Pubitemid 32519656)
20. Sattler M, Schleucher J, Griesinger C (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Progress in Nuclear Magnetic Resonance Spectroscopy 34: 93-158. (Pubitemid 129595216)
21. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
22. Goddard TD, Kneller DG (2008) SPARKY 3. University of California, San Francisco.
23. Shen Y, Delaglio F, Cornilescu G, Bax A (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 44: 213-223.
24. Brunger AT (2007) Version 1.2 of the Crystallography and NMR system. Nat Protoc 2: 2728-2733.
25. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486. (Pubitemid 126706801)
26. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, et al. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33: 5984-6003. (Pubitemid 24184605)
27. Kay LE, Torchia DA, Bax A (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28: 8972-8979. (Pubitemid 19283459)
28. Hura GL, Menon AL, Hammel M, Rambo RP, Poole FL, et al. (2009) Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS). Nat Methods 6: 606-612.
29. Putnam CD, Hammel M, Hura GL, Tainer JA (2007) X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q Rev Biophys 40: 191-285. (Pubitemid 350261954)
30. Rambo RP, Tainer JA (2011) Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law. Biopolymers 95: 559-571.
31. Svergun DI (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76: 2879-2886.
32. Schneidman-Duhovny D, Hammel M, Sali A (2010) FoXS: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res 38: W540-544.
33. Pelikan M, Hura GL, Hammel M (2009) Structure and flexibility within proteins as identified through small angle X-ray scattering. Gen Physiol Biophys 28: 174-189.
34. Hammel M (2012) Validation of macromolecular flexibility in solution by small-angle X-ray scattering (SAXS). Eur Biophys J 41: 789-799.
35. Thompson J, Higgins D, Gibson T (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680. (Pubitemid 24354800)
36. Gouet P, Courcelle E, Stuart D, Métoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308. (Pubitemid 29213756)
37. Zemla A (2003) LGA: A method for finding 3D similarities in protein structures. Nucleic Acids Res 31: 3370-3374.
38. Bernstein FC, Koetzle TF, Williams GJ, Meyer EF, Brice MD, et al. (1977) The Protein Data Bank. A computer-based archival file for macromolecular structures. Eur J Biochem 80: 319-324. (Pubitemid 8218202)
39. DeLano WL (2002) The PyMOL Molecular Graphics System. 2009: http://www.pymol.org.
40. Rocchia W, Sridharan S, Nicholls A, Alexov E, Chiabrera A, et al. (2002) Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects. J Comput Chem 23: 128-137. (Pubitemid 34063137)
41. Blanco AG, Sola M, Gomis-Rüth FX, Coll M (2002) Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 10: 701-713.
42. Okamura H, Hanaoka S, Nagadoi A, Makino K, Nishimura Y (2000) Structural comparison of the PhoB and OmpR DNA-binding/transactivation domains and the arrangement of PhoB molecules on the phosphate box. J Mol Biol 295: 1225-1236.
43. Rhee JE, Sheng W, Morgan LK, Nolet R, Liao X, et al. (2008) Amino acids important for DNA recognition by the response regulator OmpR. J Biol Chem 283: 8664-8677.
44. Chen Y, Abdel-Fattah WR, Hulett FM (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: 1493-1502. (Pubitemid 38248740)
45. Narayanan A, Paul LN, Tomar S, Patil DN, Kumar P, et al. (2012) Structure-function studies of DNA binding domain of response regulator KdpE reveals equal affinity interactions at DNA half-sites. PLoS One 7: e30102.
46. Kondo H, Nakagawa A, Nishihira J, Nishimura Y, Mizuno T, et al. (1997) Escherichia coli positive regulator OmpR has a large loop structure at the putative RNA polymerase interaction site. Nat Struct Biol 4: 28-31. (Pubitemid 27020919)
47. Wang S, Engohang-Ndong J, Smith I (2007) Structure of the DNA-binding domain of the response regulator PhoP from Mycobacterium tuberculosis. Biochemistry 46: 14751-14761. (Pubitemid 350308867)
48. Gupta SS, Borin BN, Cover TL, Krezel AM (2009) Structural analysis of the DNA-binding domain of the Helicobacter pylori response regulator ArsR. J Biol Chem 284: 6536-6545.
49. Makino K, Amemura M, Kim SK, Nakata A, Shinagawa H (1993) Role of the sigma 70 subunit of RNA polymerase in transcriptional activation by activator protein PhoB in Escherichia coli. Genes Dev 7: 149-160. (Pubitemid 23071208)
50. Makino K, Amemura M, Kawamoto T, Kimura S, Shinagawa H, et al. (1996) DNA binding of PhoB and its interaction with RNA polymerase. J Mol Biol 259: 15-26. (Pubitemid 26162618)
51. Tsung K, Brissette RE, Inouye M (1990) Enhancement of RNA polymerase binding to promoters by a transcriptional activator, OmpR, in Escherichia coli: its positive and negative effects on transcription. Proc Natl Acad Sci U S A 87: 5940-5944.
52. Schär J, Sickmann A, Beier D (2005) Phosphorylation-independent activity of atypical response regulators of Helicobacter pylori. J Bacteriol 187: 3100-3109. (Pubitemid 40571603)
53. Fraser JS, Merlie JP, Echols N, Weisfield SR, Mignot T, et al. (2007) An atypical receiver domain controls the dynamic polar localization of the Myxococcus xanthus social motility protein FrzS. Mol Microbiol 65: 319-332. (Pubitemid 47052716)
54. Rambo RP, Tainer JA (2013) Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496: 477-481.
55. Rambo RP, Tainer JA (2013) Super-resolution in solution X-ray scattering and its applications to structural systems biology. Annu Rev Biophys 42: 415-441.
56. Mertens HD, Svergun DI (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J Struct Biol 172: 128-141.
57. Schneidman-Duhovny D, Hammel M, Tainer JA, Sali A (2013) Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments. Biophys J 105: 962-974.
58. Bernadó P, Svergun DI (2012) Analysis of intrinsically disordered proteins by small-angle X-ray scattering. Methods Mol Biol 896: 107-122.
59. Bernadó P, Svergun DI (2012) Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering. Mol Biosyst 8: 151-167.
60. Hura GL, Budworth H, Dyer KN, Rambo RP, Hammel M, et al. (2013) Comprehensive macromolecular conformations mapped by quantitative SAXS analyses. Nat Methods 10: 453-454.
61. Biersmith BH, Hammel M, Geisbrecht ER, Bouyain S (2011) The immunoglobulin-like domains 1 and 2 of the protein tyrosine phosphatase LAR adopt an unusual horseshoe-like conformation. J Mol Biol 408: 616-627.
62. Chen H, Ricklin D, Hammel M, Garcia BL, McWhorter WJ, et al. (2010) Allosteric inhibition of complement function by a staphylococcal immune evasion protein. Proc Natl Acad Sci U S A 107: 17621-17626.
63. Duda DM, Olszewski JL, Tron AE, Hammel M, Lambert LJ, et al. (2012) Structure of a glomulin-RBX1-CUL1 complex: inhibition of a RING E3 ligase through masking of its E2-binding surface. Mol Cell 47: 371-382.
64. Liu X, Hammel M, He Y, Tainer JA, Jeng US, et al. (2013) Structural insights into the interaction of IL-33 with its receptors. Proc Natl Acad Sci U S A.
65. Abbas YM, Pichlmair A, Górna MW, Superti-Furga G, Nagar B (2013) Structural basis for viral 59-PPP-RNA recognition by human IFIT proteins. Nature 494: 60-64.
66. Koch MH, Vachette P, Svergun DI (2003) Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q Rev Biophys 36: 147-227. (Pubitemid 37493573)
67. Eswar N, Eramian D, Webb B, Shen MY, Sali A (2008) Protein structure modeling with MODELLER. Methods Mol Biol 426: 145-159.
68. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
69. Wing R, Drew H, Takano T, Broka C, Tanaka S, et al. (1980) Crystal structure analysis of a complete turn of B-DNA. Nature 287: 755-758.
70. Luscombe NM, Laskowski RA, Thornton JM (2001) Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res 29: 2860-2874. (Pubitemid 32685051)
71. Toro-Roman A, Wu T, Stock AM (2005) A common dimerization interface in bacterial response regulators KdpE and TorR. Protein Sci 14: 3077-3088. (Pubitemid 41770148)
72. Toro-Roman A, Mack TR, Stock AM (2005) 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: 11-26. (Pubitemid 40616445)
73. Bachhawat P, Swapna GV, Montelione GT, Stock AM (2005) Mechanism of activation for transcription factor PhoB suggested by different modes of dimerization in the inactive and active states. Structure 13: 1353-1363. (Pubitemid 41262102)
74. Blanco AG, Canals A, Bernues J, Sola M, Coll M (2011) The structure of a transcription activation subcomplex reveals how sigma(70) is recruited to PhoB promoters. EMBO J 30: 3776-3785.
75. Delany I, Spohn G, Rappuoli R, 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: 4800-4810.
76. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR, et al. (2011) Development of a transformation system for Chlamydia trachomatis: restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector. PLoS Pathog 7: e1002258.
77. Kari L, Goheen MM, Randall LB, Taylor LD, Carlson JH, et al. (2011) Generation of targeted Chlamydia trachomatis null mutants. Proc Natl Acad Sci U S A 108: 7189-7193.
78. Bauler LD, Hackstadt T (2014) Expression and Targeting of Secreted Proteins from Chlamydia trachomatis. J Bacteriol.
79. Wickstrum J, Sammons LR, Restivo KN, Hefty PS (2013) Conditional gene expression in Chlamydia trachomatis using the tet system. PLoS One 8: e76743.
80. Johnson CM, Fisher DJ (2013) Site-Specific, Insertional Inactivation of incA in Chlamydia trachomatis Using a Group II Intron. PLoS One 8: e83989.