The linker between the dimerization and catalytic domains of the CheA histidine kinase propagates changes in structure and dynamics that are important for enzymatic activity

Biochemistry

Volumn 53, Issue 5, 2014, Pages 855-861

  Wang, Xiqing ^a   Vallurupalli, Pramodh ^b   Vu, Anh ^a   Lee, Kwangwoon ^a   Sun, Sheng ^a   Bai, Wen Ju ^a   Wu, Chun ^a   Zhou, Hongjun ^a   Shea, Joan Emma ^a   Kay, Lewis E ^b   Dahlquist, Frederick W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEINS; CATALYTIC DOMAIN; ENZYME ACTIVATION; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN MULTIMERIZATION; THERMOTOGA MARITIMA;

EID: 84894213356     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4012379     Document Type: Article

References (54)

1. Krell, T., Lacal, J., Busch, A., Silva-Jimenez, H., Guazzaroni, M., and Ramos, J. L. (2010) Bacterial sensor kinases: Diversity in the recognition of environmental signals Annu. Rev. Microbiol. 64, 539-559
2. Watanabe, T., Okada, A., Gotoh, Y., and Utsumi, R. (2008) Inhibitors targeting two-component signal transduction Adv. Exp. Med. Biol. 631, 229-236
3. Barrett, J. F. and Hoch, J. A. (1998) Two-component signal transduction as a target for microbial anti-infective therapy Antimicrob. Agents Chemother. 42, 1529-1536
4. Kurosu, M. and Begari, E. (2010) Bacterial protein kinase inhibitors Drug Dev. Res. 71, 168-187
5. Josenhans, C. and Suerbaum, S. (2002) The role of motility as a virulence factor in bacteria Int. J. Med. Microbiol. 291, 605-614
6. Lertsethtakarn, P., Ottemann, K. M., and Hendrixson, D. R. (2011) Motility and chemotaxis in Campylobacter and Helicobacter Annu. Rev. Microbiol. 65, 389-410
7. Butler, S. M. and Camilli, A. (2005) Going against the grain: Chemotaxis and infection in Vibrio cholerae Nat. Rev. Microbiol. 3, 611-620
8. Lux, R. and Shi, W. (2004) Chemotaxis-guided movements in bacteria Crit. Rev. Oral Biol. Med. 15, 207-220
9. Wadhams, G. H. and Armitage, J. P. (2004) Making sense of it all: Bacterial chemotaxis Nat. Rev. Mol. Cell Biol. 5, 1024-1037
10. Hazelbauer, G. L., Falke, J. J., and Parkinson, J. S. (2008) Bacterial chemoreceptors: High-performance signaling in networked arrays Trends Biochem. Sci. 33, 9-19
11. Swanson, R. V., Bourret, R. B., and Simon, M. I. (1993) Intermolecular complementation of the kinase activity of CheA Mol. Microbiol. 8, 435-441
12. Borkovich, K. A., Kaplan, N., Hess, J. F., and Simon, M. I. (1989) Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer Proc. Natl. Acad. Sci. U.S.A. 86, 1208-1212
13. Gegner, J. A., Graham, D. R., Roth, A. F., and Dahlquist, F. W. (1992) Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway Cell 70, 975-982
14. Bourret, R. B., Davagnino, J., and Simon, M. I. (1993) The carboxy-terminal portion of the CheA kinase mediates regulation of autophosphorylation by transducer and CheW J. Bacteriol. 175, 2097-2101
15. Garzón, A. and Parkinson, J. S. (1996) Chemotactic signaling by the P1 phosphorylation domain liberated from the CheA histidine kinase of Escherichia coli J. Bacteriol. 178, 6752-6758
16. Bilwes, A. M., Alex, L. A., Crane, B. R., and Simon, M. I. (1999) Structure of CheA, a signal-transducing histidine kinase Cell 96, 131-141
17. Bilwes, A. M., Quezada, C. M., Croal, L. R., Crane, B. R., and Simon, M. I. (2001) Nucleotide binding by the histidine kinase CheA Nat. Struct. Biol. 8, 353-360
18. Miller, A. S., Kohout, S. C., Gilman, K. A., and Falke, J. J. (2006) CheA kinase of bacterial chemotaxis: Chemical mapping of four essential docking sites Biochemistry 45, 8699-8711
19. Francis, N. R., Wolanin, P. M., Stock, J. B., Derosier, D. J., and Thomas, D. R. (2004) Three-dimensional structure and organization of a receptor/signaling complex Proc. Natl. Acad. Sci. U.S.A. 101, 17480-17485
20. Zhao, J. and Parkinson, J. S. (2006) Cysteine-scanning analysis of the chemoreceptor-coupling domain of the Escherichia coli chemotaxis signaling kinase CheA J. Bacteriol. 188, 4321-4330
21. Park, S. Y., Borbat, P. P., Gonzalez-Bonet, G., Bhatnagar, J., Pollard, A. M., Freed, J. H., Bilwes, A. M., and Crane, B. R. (2006) Reconstruction of the chemotaxis receptor-kinase assembly Nat. Struct. Mol. Biol. 13, 400-407
22. Bhatnagar, J., Borbat, P. P., Pollard, A. M., Bilwes, A. M., Freed, J. H., and Crane, B. R. (2010) Structure of the ternary complex formed by a chemotaxis receptor signaling domain, the CheA histidine kinase, and the coupling protein CheW as determined by pulsed dipolar ESR spectroscopy Biochemistry 49, 3824-3841
23. Briegel, A., Li, X., Bilwes, A. M., Hughes, K. T., Jensen, G. J., and Crane, B. R. (2012) Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins Proc. Natl. Acad. Sci. U.S.A. 109, 3766-3771
24. Vu, A., Wang, X., Zhou, H., and Dahlquist, F. W. (2012) The receptor-CheW binding interface in bacterial chemotaxis J. Mol. Biol. 415, 759-767
25. Wang, X., Vu, A., Lee, K., and Dahlquist, F. W. (2012) CheA-receptor interaction sites in bacterial chemotaxis J. Mol. Biol. 422, 282-290
26. Liu, J., Hu, B., Morado, D. R., Jani, S., Manson, M. D., and Margolin, W. (2012) Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells Proc. Natl. Acad. Sci. U.S.A. 109, E1481-E1488
27. Li, X., Fleetwod, A. D., Bayas, C., Bilwes, A. M., Ortega, D. R., Falke, J. J., Zhulin, I. B., and Crane, B. R. (2013) The 3.2 Å Resolution Structure of a Receptor:CheA:CheW Signaling Complex Defines Overlapping Binding Sites and Key Residue Interactions within Bacterial Chemosensory Arrays Biochemistry 52, 3852-3865
28. Piasta, K. N., Ulliman, C. J., Slivka, P. F., Crane, B. R., and Falke, J. J. (2013) Defining a Key Receptor-CheA Kinase Contact and Elucidating Its Function in the Membrane-Bound Bacterial Chemosensory Array: A Disulfide Mapping and TAM-IDS Study Biochemistry 52, 3866-3880
29. Wang, X., Wu, C., Vu, A., Shea, J.-E., and Dahlquist, F. W. (2012) Computational and experimental analyses reveal the essential roles of interdomain linkers in the biological function of chemotaxis histidine kinase CheA J. Am. Chem. Soc. 134, 16107-16110
30. Ames, P. and Parkinson, J. S. (1994) Constitutively signaling fragments of Tsr, the Escherichia coli serine chemoreceptor J. Bacteriol. 176, 6340-6348
31. Stock, A., Chen, T., Welsh, D., and Stock, J. (1988) CheA protein, a central regulator of bacterial chemotaxis, belongs to a family of proteins that control gene expression in response to changing environmental conditions Proc. Natl. Acad. Sci. U.S.A. 85, 1403-1407
32. Gegner, J. A. and Dahlquist, F. W. (1991) Signal transduction in bacteria: CheW forms a reversible complex with the protein kinase CheA Proc. Natl. Acad. Sci. U.S.A. 88, 750-754
33. Lowry, D. F., Roth, A. F., Rupert, P. B., Dahlquist, F. W., Moy, F. J., Domaille, P. J., and Matsumura, P. (1994) Signal transduction in chemotaxis. A propagating conformation change upon phosphorylation of CheY J. Biol. Chem. 269, 26358-26362
34. Salzmann, M., Wider, G., Pervushin, K., Senn, H., and Wüthrich, K. (1999) TROSY-type Triple-Resonance Experiments for Sequential NMR Assignments of Large Proteins J. Am. Chem. Soc. 121, 844-848
35. Salzmann, M., Pervushin, K., Wider, G., Senn, H., and Wüthrich, K. (1998) TROSY in triple-resonance experiments: New perspectives for sequential NMR assignment of large proteins Proc. Natl. Acad. Sci. U.S.A. 95, 13585-13590
36. Hamel, D. J., Zhou, H., Starich, M. R., Byrd, R. A., and Dahlquist, F. W. (2006) Chemical-shift-perturbation mapping of the phosphotransfer and catalytic domain interaction in the histidine autokinase CheA from Thermotoga maritima Biochemistry 45, 9509-9517
37. Loria, J. P., Rance, M., and Palmer, A. G. (1999) A relaxation- compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy J. Am. Chem. Soc. 121, 2331-2332
38. Ishima, R., Wingfield, P. T., Stahl, S. J., Kaufman, J. D., and Torchia, D. A. (1998) Using amide H-1 and N-15 transverse relaxation to detect millisecond time-scale motions in perdeuterated proteins: Application to HIV-1 protease J. Am. Chem. Soc. 120, 10534-10542
39. 15N relaxation dispersion NMR spectroscopy: Application to Asn and Gln residues in a cavity mutant of T4 lysozyme J. Am. Chem. Soc. 123, 967-975
40. Loria, J. P., Rance, M., and Palmer, A. G. (1999) A TROSY CPMG sequence for characterizing chemical exchange in large proteins J. Biomol. NMR 15, 151-155
41. Vallurupalli, P., Hansen, D. F., Stollar, E., Meirovitch, E., and Kay, L. E. (2007) Measurement of bond vector orientations in invisible excited states of proteins Proc. Natl. Acad. Sci. U.S.A. 104, 18473-18477
42. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A Multidimensional Spectral Processing System Based on Unix Pipes J. Biomol. NMR 6, 277-293
43. Goddard, T. D. and Kneller, D. G. (2000) SPARKY 3, University of California, San Francisco.
44. Ninfa, E. G., Stock, A., Mowbray, S., and Stock, J. (1991) Reconstitution of the bacterial chemotaxis signal transduction system from purified components J. Biol. Chem. 266, 9764-9770
45. Stewart, R. C., VanBruggen, R., Ellefson, D. D., and Wolfe, A. J. (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, 12269-12279
46. Swanson, R. V., Sanna, M. G., and Simon, M. I. (1996) Thermostable chemotaxis proteins from the hyperthermophilic bacterium Thermotoga maritima J. Bacteriol. 178, 484-489
47. Pervushin, K., Riek, R., Wider, G., and Wüthrich, K. (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution Proc. Natl. Acad. Sci. U.S.A. 94, 12366-12371
48. Palmer, A. G., Kroenke, C. D., and Loria, J. P. (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules Methods Enzymol. 339, 204-238
49. Gloor, S. L. and Falke, J. J. (2009) Thermal domain motions of CheA kinase in solution: Disulfide trapping reveals the motional constraints leading to trans-autophosphorylation Biochemistry 48, 3631-3644
50. Nishiyama, S., Garzon, A., and Parkinson, J. S. (2014) Mutational analysis of the P1 phosphorylation domain in Escherichia coli CheA, the signaling kinase for chemotaxis J. Bacteriol. 196, 257-264
51. Zhang, J., Xu, Y., Shen, J., Luo, X., Chen, J., Chen, K., Zhu, W., and Jiang, H. (2005) Dynamic mechanism for the autophosphorylation of CheA histidine kinase: Molecular dynamics simulations J. Am. Chem. Soc. 127, 11709-11719
52. Kim, K. K., Yokota, H., and Kim, S.-H. (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor Nature 400, 787-792
53. Zhou, Q., Ames, P., and Parkinson, J. S. (2009) Mutational analyses of HAMP helices suggest a dynamic bundle model of input-output signalling in chemoreceptors Mol. Microbiol. 73, 801-814
54. Swain, K. E., Gonzalez, M. A., and Falke, J. J. (2009) 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, 9266-9277