Sensor domain of histidine kinase kinb of pseudomonas a helix-swapped dimer

Journal of Biological Chemistry

Volumn 289, Issue 18, 2014, Pages 12232-12244

  Tan, Kemin ^a,b   Chhor, Gekleng ^a   Binkowski, T Andrew ^a   Jedrzejczak, Robert P ^a   Makowska Grzyska, Magdalena ^b   Joachimiak, Andrzej ^a,b  

^a ARGONNE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIOPHAGES; ENZYMES; LIGANDS; SIGNAL TRANSDUCTION;

DIMER INTERFACE; HISTIDINE KINASE; LIGAND BINDING; LIGAND-FREE; SENSOR DOMAINS; SIGNALING MOLECULES; STRUCTURE FORMS;

DIMERS;

ALGINIC ACID; DIMER; FRUCTOSE 6 PHOSPHATE; MANNOSE 6 PHOSPHATE; PROTEIN HISTIDINE KINASE; PROTEIN HISTIDINE KINASE KINB; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; COMPUTER MODEL; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME STRUCTURE; GENETIC CONSERVATION; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR STABILITY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PSEUDOMONAS; RESIDUE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

ALGINATE BIOSYNTHESIS; BACTERIAL SIGNAL TRANSDUCTION; BIOSENSORS; HELIX-SWAPPED DIMER; HISTIDINE KINASES; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SENSOR DOMAIN; TWO-COMPONENT SYSTEM;

ALGINATES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; FRUCTOSEPHOSPHATES; GLUCURONIC ACID; HEXURONIC ACIDS; LIGANDS; MANNOSEPHOSPHATES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN KINASES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

EID: 84899759953     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.514836     Document Type: Article

References (59)

1. Govan, J. R., and Deretic, V. (1996) Microbial pathogenesis in cystic fibrosis: Mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60, 539-574
2. Deretic, V., Gill, J. F., and Chakrabarty, A. M. (1987) Gene algD coding for GDP mannose dehydrogenase is transcriptionally activated in mucoid Pseudomonas aeruginosa. J. Bacteriol. 169, 351-358
3. Martin, D. W., Schurr, M. J., Mudd, M. H., Govan, J. R., Holloway, B. W., and Deretic, V. (1993) Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. U.S.A. 90, 8377-8381
4. Mathee, K., McPherson, C. J., and Ohman, D. E. (1997) Posttranslational control of the algT (algU)-encoded-22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN). J. Bacteriol. 179, 3711-3720
5. Damron, F. H., Qiu, D., and Yu, H. D. (2009) The Pseudomonas aeruginosa sensor kinase KinB negatively controls alginate production through AlgW-dependent MucA proteolysis. J. Bacteriol. 191, 2285-2295
6. Parkinson, J. S., and Kofoid, E. C. (1992) Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26, 71-112
7. Ma, S., Wozniak, D. J., and Ohman, D. E. (1997) Identification of the histidine protein kinase KinB in Pseudomonas aeruginosa and its phosphorylation of the alginate regulator algB. J. Biol. Chem. 272, 17952-17960
8. Gooderham, W. J., and Hancock, R. E. (2009) Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 33, 279-294
9. Damron, F. H., Owings, J. P., Okkotsu, Y., Varga, J. J., Schurr, J. R., Goldberg, J. B., Schurr, M. J., and Yu, H. D. (2012) Analysis of the Pseudomonas aeruginosa regulon controlled by the sensor kinase KinB and factor RpoN. J. Bacteriol. 194, 1317-1330
10. Chand, N. S., and Hung, D. T. (2011) The two-component sensor kinase KinB acts as a non-canonical switch between acute and chronic infection. Virulence 2, 553-558
11. Chand, N. S., Lee, J. S., Clatworthy, A. E., Golas, A. J., Smith, R. S., and Hung, D. T. (2011) The sensor kinase KinB regulates virulence in acute Pseudomonas aeruginosa infection. J. Bacteriol. 193, 2989-2999
12. Chand, N. S., Clatworthy, A. E., and Hung, D. T. (2012) The two-component sensor KinB acts as a phosphatase to regulate Pseudomonas aeruginosa Virulence. J. Bacteriol. 194, 6537-6547
13. Gao, R., and Stock, A. M. (2009) Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63, 133-154
14. Cheung, J., and Hendrickson, W. A. (2010) Sensor domains of two-component regulatory systems. Curr. Opin. Microbiol. 13, 116-123
15. Perry, J., Koteva, K., and Wright, G. (2011) Receptor domains of twocomponent signal transduction systems. Mol. Biosyst. 7, 1388-1398
16. Reinelt, S., Hofmann, E., Gerharz, T., Bott, M., and Madden, D. R. (2003) The structure of the periplasmic ligand-binding domain of the sensor kinase CitA reveals the first extracellular PAS domain. J. Biol. Chem. 278, 39189-39196
17. Cheung, J., Bingman, C. A., Reyngold, M., Hendrickson, W. A., and Waldburger, C. D. (2008) Crystal structure of a functional dimer of the PhoQ sensor domain. J. Biol. Chem. 283, 13762-13770
18. Cho, U. S., Bader, M. W., Amaya, M. F., Daley, M. E., Klevit, R. E., Miller, S. I., and Xu, W. (2006) Metal bridges between the PhoQ sensor domain and the membrane regulate transmembrane signaling. J. Mol. Biol. 356, 1193-1206
19. Pappalardo, L., Janausch, I. G., Vijayan, V., Zientz, E., Junker, J., Peti, W., Zweckstetter, M., Unden, G., and Griesinger, C. (2003) The NMR structure of the sensory domain of the membranous two-component fumarate sensor (histidine protein kinase) DcuS of Escherichia coli. J. Biol. Chem. 278, 39185-39188
20. Neiditch, M. B., Federle, M. J., Miller, S. T., Bassler, B. L., and Hughson, F. M. (2005) Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol. Cell 18, 507-518
21. Zhou, Y. F., Nan, B., Nan, J., Ma, Q., Panjikar, S., Liang, Y. H., Wang, Y., and Su, X. D. (2008) C4-dicarboxylates sensing mechanism revealed by the crystal structures of DctB sensor domain. J. Mol. Biol. 383, 49-61
22. Cheung, J., and Hendrickson, W. A. (2008) Crystal structures of C4-dicarboxylate ligand complexes with sensor domains of histidine kinases DcuS and DctB. J. Biol. Chem. 283, 30256-30265
23. Wu, R., Gu, M., Wilton, R., Babnigg, G., Kim, Y., Pokkuluri, P. R., Szurmant, H., Joachimiak, A., and Schiffer, M. (2013) Insight into the sporulation phosphorelay: Crystal structure of the sensor domain of Bacillus subtilis histidine kinase, KinD. Protein Sci. 22, 564-576
24. Chang, C., Tesar, C., Gu, M., Babnigg, G., Joachimiak, A., Pokkuluri, P. R., Szurmant, H., and Schiffer, M. (2010) Extracytoplasmic PAS-like domains are common in signal transduction proteins. J. Bacteriol. 192, 1156-1159
25. Cheung, J., and Hendrickson, W. A. (2009) Structural analysis of ligand stimulation of the histidine kinase NarX. Structure 17, 190-201
26. Moore, J. O., and Hendrickson, W. A. (2009) Structural analysis of sensor domains from the TMAO-responsive histidine kinase receptor TorS. Structure 17, 1195-1204
27. Ulrich, L. E., and Zhulin, I. B. (2005) Four-helix bundle: A ubiquitous sensory module in prokaryotic signal transduction. Bioinformatics 21, Suppl. 3:iii45-48
28. Cheung, J., Le-Khac, M., and Hendrickson, W. A. (2009) Crystal structure of a histidine kinase sensor domain with similarity to periplasmic binding proteins. Proteins 77, 235-241
29. Herrou, J., Bompard, C., Wintjens, R., Dupr, E., Willery, E., Villeret, V., Locht, C., Antoine, R., and Jacob-Dubuisson, F. (2010) Periplasmic domain of the sensor-kinase BvgS reveals a new paradigm for the Venus flytrap mechanism. Proc. Natl. Acad. Sci. U.S.A. 107, 17351-17355
30. Stibitz, S. (2007) in Bordetella Molecular Biology (Locht, C., ed) pp. 47-68, Horizon Bioscience, Norfolk, United Kingdom
31. Lowe, E. C., Basl, A., Czjzek, M., Firbank, S. J., and Bolam, D. N. (2012) A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system. Proc. Natl. Acad. Sci. U.S.A. 109, 7298-7303
32. Rocchetta, H. L., Burrows, L. L., and Lam, J. S. (1999) Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 63, 523-553
33. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L., and Clardy, J. (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105-124
34. Kim, Y., Dementieva, I., Zhou, M., Wu, R., Lezondra, L., Quartey, P., Joachimiak, G., Korolev, O., Li, H., and Joachimiak, A. (2004) Automation of protein purification for structural genomics. J. Struct. Funct. Genomics 5, 111-118
35. Klock, H. E., and Lesley, S. A. (2009) The polymerase incomplete primer extension (PIPE) method applied to high-throughput cloning and sitedirected mutagenesis. Methods Mol. Biol. 498, 91-103
36. Eschenfeldt, W. H., Makowska-Grzyska, M., Stols, L., Donnelly, M. I., Jedrzejczak, R., and Joachimiak, A. (2013) New LIC vectors for production of proteins from genes containing rare codons. J. Struct. Funct. Genomics 14, 135-144
37. Rosenbaum, G., Alkire, R. W., Evans, G., Rotella, F. J., Lazarski, K., Zhang, R. G., Ginell, S. L., Duke, N., Naday, I., Lazarz, J., Molitsky, M. J., Keefe, L., Gonczy, J., Rock, L., Sanishvili, R., Walsh, M. A., Westbrook, E., and Joachimiak, A. (2006) The structural biology center 19ID undulator beamline: facility specifications and protein crystallographic results. J. Synchrotron Radiat. 13, 30-45
38. Minor, W., Cymborowski, M., Otwinowski, Z., and Chruszcz, M. (2006) HKL-3000: the integration of data reduction and structure solution-From diffraction images to an initial model in minutes. Acta Crystallogr. D Biol. Crystallogr. 62, 859-866
39. Schneider, T. R., and Sheldrick, G. M. (2002) Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779
40. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
41. Cohen, S. X., Morris, R. J., Fernandez, F. J., Ben Jelloul, M., Kakaris, M., Parthasarathy, V., Lamzin, V. S., Kleywegt, G. J., and Perrakis, A. (2004) Towards complete validated models in the next generation of ARP/wARP. Acta Crystallogr. D Biol. Crystallogr. 60, 2222-2229
42. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
43. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
44. Vagin, A., and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25
45. Shiba, K., Niidome, T., Katoh, E., Xiang, H., Han, L., Mori, T., and Katayama, Y. (2010) Polydispersity as a parameter for indicating the thermal stability of proteins by dynamic light scattering. Anal. Sci. 26, 659-663
46. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242
47. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
48. Lee, D., Lee, J., and Seok, C. (2013) What stabilizes close arginine pairing in proteins? Phys. Chem. Chem. Phys. 15, 5844-5853
49. Kulik, V., Weyand, M., Seidel, R., Niks, D., Arac, D., Dunn, M. F., and Schlichting, I. (2002) On the role of-Thr183 in the allosteric regulation and catalytic mechanism of tryptophan synthase. J. Mol. Biol. 324, 677-690
50. Soetens, J.-C., Millot, C., Chipot, C., Jansen, G., J. , Angyán, J., and Maigret, B. (1997) Effect of polarizability on the potential of mean fluorescence of two cations. The guanidinium-guanidinium ion pair in water. J. Phys. Chem. B 101, 10910-10917
51. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
52. Lin, S. L., Tsai, C. J., and Nussinov, R. (1995) A study of four-helix bundles: investigating protein folding via similar architectural motifs in protein cores and in subunit interfaces. J. Mol. Biol. 248, 151-161
53. Milburn, M. V., Privé, G. G., Milligan, D. L., Scott, W. G., Yeh, J., Jancarik, J., Koshland, D. E., Jr., and Kim, S. H. (1991) Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science 254, 1342-1347
54. Nettleship, J. E., Brown, J., Groves, M. R., and Geerlof, A. (2008) Methods for protein characterization by mass spectrometry, thermal shift (ThermoFluor) assay, and multiangle or static light scattering. Methods Mol. Biol. 426, 299-318
55. Pawar, S. N., and Edgar, K. J. (2012) Alginate derivatization: a review of chemistry, properties and applications. Biomaterials 33, 3279-3305
56. Cimmperman, P., Baranauskiene, L., Jachimoviciute, S., Jachno, J., Torresan, J., Michailoviene, V., Matuliene, J., Sereikaite, J., Bumelis, V., and Matulis, D. (2008) A quantitative model of thermal stabilization and destabilization of proteins by ligands. Biophys. J. 95, 3222-3231
57. Neiditch, M. B., Federle, M. J., Pompeani, A. J., Kelly, R. C., Swem, D. L., Jeffrey, P. D., Bassler, B. L., and Hughson, F. M. (2006) Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126, 1095-1108
58. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
59. Gouet, P., Courcelle, E., Stuart, D. I., and Métoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308