Solution structure of a complex of the histidine autokinase CheA with its substrate CheY

Biochemistry

Volumn 51, Issue 18, 2012, Pages 3786-3798

  Mo, Guoya ^a   Zhou, Hongjun ^a   Kawamura, Tetsuya ^a   Dahlquist, Frederick W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CHEMOTAXIS; CATALYTIC DOMAINS; COMPLEX STRUCTURE; E. COLI; FLAGELLAR MOTORS; HISTIDINE-CONTAINING PHOSPHOTRANSFER; NUCLEAR MAGNETIC RESONANCE TECHNIQUES; PHOSPHO-TRANSFER; PHOSPHORYL GROUPS; RELATIVE ORIENTATION; RESPONSE REGULATORS; SIGNALING SYSTEMS; SOLUTION STRUCTURES; STRUCTURAL BASIS; TWO-COMPONENT;

BIOCHEMISTRY; CYTOLOGY; ESCHERICHIA COLI; MUTAGENESIS; PHOSPHORYLATION; PLANTS (BOTANY);

AMINO ACIDS;

CHEA KINASE; CHEY PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMOTAXIS; CRYSTAL STRUCTURE; ENZYME STRUCTURE; ESCHERICHIA COLI; FLAGELLUM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHATE TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; RHODOBACTER SPHAEROIDES; SALMONELLA TYPHIMURIUM; YEAST;

BACTERIAL PROTEINS; KINETICS; MEMBRANE PROTEINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84860750796     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300147m     Document Type: Article

References (51)

1. Stock, A. M., Robinson, V. L., and Goudreau, P. N. (2000) Two-component signal transduction Annu. Rev. Biochem. 69, 183-215
2. Hamel, D. J., Zhou, H., Starich, M. R., Byrd, 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 (31) 9509-9517 (Pubitemid 44223254)
3. Baker, M. D., Wolanin, P. M., and Stock, J. B. (2006) Systems biology of bacterial chemotaxis Curr. Opin. Microbiol. 9, 187-192
4. Baker, M. D., Wolanin, P. M., and Stock, J. B. (2006) Signal transduction in bacterial chemotaxis BioEssays 28, 9-22
5. Schuster, M., Silversmith, R. E., and Bourret, R. B. (2001) Conformational coupling in the chemotaxis response regulator CheY Proc. Natl. Acad. Sci. U.S.A. 98 (11) 6003-6008 (Pubitemid 32488183)
6. Shukla, D. and Matsumura, P. (1995) Mutation leading to altered CheA binding cluster on a Face of CheY J. Biol. Chem. 270 (41) 24414-24419
7. Mayover, T. L., Halkides, C. J., and Stewart, R. C. (1999) Kinetic characterization of CheY phosphorylation reactions: Comparison of P-CheA and small-molecule phosphodonors Biochemistry 38 (8) 2259-2271
8. Zhou, H. Z., McEvoy, M. M., Lowry, D. F., Swanson, R. V., Simon, M. I., and Dahlquist, F. W. (1996) Phosphotransfer and CheY-binding domains of the histidine autokinase CheA are joined by a flexible linker Biochemistry 35 (2) 433-443 (Pubitemid 26033914)
9. Zapf, J., Sen, U., Madhusuda, Hoch, J. A., and Varughese, K. I. (2000) A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction Structure 8 (8) 851-862
10. Casino, P., Rubio, V., and Marina, A. (2009) Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction Cell 139, 325-336
11. Xu, Q., Porter, S. W., and West, A. H. (2003) The yeast YPD1/SLN1 complex: iInsights into molecular recognition in two-component signaling systems Structure 11, 1569-1581 (Pubitemid 37510356)
12. Bell, C. H., Porter, S. L., Strawson, A., Stuart, D. I., and Armitage, J. P. (2010) Using structural information to change the phosphotransfer specificity of a two-component chemotaxis signaling complex PLoS Biol. 8 (2) e1000306
13. Battiste, J. L. and Wagner, G. (2000) Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear Overhauser effect data Biochemistry 39, 5355-5365 (Pubitemid 30257075)
14. Peterson, D. W., Zhou, H., Dahlquist, F. W., and Lew, J. (2008) A soluble oligomer of Tau associated with fiber formation analyzed by NMR Biochemistry 47 (28) 7393-7404 (Pubitemid 351991018)
15. Lowry, D. F., Roth, A. F., Rupert, P. B., and Dahlquist, F. W. (1994) Signal transduction in chemotaxis J. Biol. Chem. 269 (42) 26358-26362
16. Swanson, R. W., Schuster, S. C., and Simon, M. I. (1993) Expression of CheA fragments which define domain encoding kinase, phosphotransfer, and cheY binding activities Biochemistry 32 (30) 7623-7629 (Pubitemid 23240804)
17. McEvoy, M. M., Hausrath, A. C., Randolph, G. B., Remington, S. J., and Dahlquist, F. W. (1998) Two binding modes reveal flexibility in kinase/response regulator interactions in the bacterial chemotaxis pathway Proc. Natl. Acad. Sci. U.S.A. 95, 7333-7338 (Pubitemid 28293252)
18. Grassetti, D. R. and Murray, J. F. (1967) The use of 2,2-dithiodipyridine in the determination of glutathione and of triphosphopyridine nucleotide by enzymatic cycling Anal. Biochem. 12, 427-434
19. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114 (26) 10663-10665
20. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMR Pipe: A multidimensional spectra; processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
21. 1H 2D NMR spectra by interactive graphics J. Magn. Reson. 24, 627-633
22. 13C decoupling J. Magn. Reson. 98, 428-435
23. Muhandiram, D. R. and Kay, L. E. (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity J. Magn. Reson., Ser. B 103, 203-216
24. Montelione, G. T., Lyons, B. A., Emerson, S. D., and Tashiro, M. (1992) An efficient triple experiment using carbon-13 isotropic mixing for determining sequence-specific resonance assignments of isotropically-enriched proteins J. Am. Chem. Soc. 114, 10974-10975
25. 13C magnetization J. Magn. Reson., Ser. B 101, 114-119
26. Logan, T. M., Olejiniczak, E. T., Xu, R. X., and Fesik, S. W. (1993) A general method for assigning NMR spectra of denatured proteins using 3D HC(CO)NH-TOCSY triple resonance experiments J. Biomol. NMR 3, 225-231
27. Clore, G. M. and Gronenborn, A. M. (1998) Determining the structures of large proteins and protein complexes by NMR Trends Biotechnol. 16, 22-34 (Pubitemid 28064815)
28. Cai, M., Huang, Y., Zheng, R., Wei, S., Ghirlando, R., Lee, M. S., Craigie, R., Gronenborn, A. M., and Clore, G. M. (1998) Solution structure of the cellular factor BAF responsible for protecting retroviral DNA from autointegration Nat. Struct. Biol. 5 (10) 903-909 (Pubitemid 28467414)
29. Kawamura, T., Le, L. U. K., Zhou, H., and Dahlquist, F. W. (2007) Solution structure of Escherichia coli PapI, a key regulator of the Pap Pili phase variation J. Mol. Biol. 365, 1130-1142 (Pubitemid 46014187)
30. Mannitol of the Escherichia coli phosphotransferase system J. Biol. Chem. 281 (13) 8939-8949 (Pubitemid 43848001)
31. r phosphoryl transfer complex between the N-terminal domain of enzyme I and HPr Nat. Struct. Biol. 6 (2) 166-173 (Pubitemid 29069780)
32. Suh, J., Iwahara, J., and Clore, G. M. (2007) Intramolecular domain- domain association/dissociation and phopsphoryl transfer in the mannitol transporter of Escherichia coli are not coupled Proc. Natl. Acad. Sci. U.S.A. 104 (9) 3153-3158 (Pubitemid 46364129)
33. Hu, J., Hu, K., Williams, D. C., Jr., Komlosh, M. E., Cai, M., and Clore, G. M. (2008) Solution NMR structure of productive and non-productive complexes between the A and B domains of the cytoplasmic subunit of the mannose transporter of the Eschericia coli phosphotransferase system J. Biol. Chem. 283 (16) 11024-11037
34. Chitobiose complex of the N, N ′-diacetylchitobiose branch of the Escherichia coli phosphertransferase system J. Biol. Chem. 285 (6) 4173-4184
35. Glucose of the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system EMBO J. 19 (21) 5635-5649
36. Mannitol and HPr of the Escherichia coli phosphotransferase system J. Biol. Chem. 277 (44) 42289-42298 (Pubitemid 35257549)
37. Glucose of the Escherichia coli glucose phosphotransferase system J. Biol. Chem. 278 (27) 25191-25206 (Pubitemid 37548684)
38. Mannose-HPr complex of the Escherichia coli mannose phosphotransferase system J. Biol. Chem. 280 (21) 20775-20784 (Pubitemid 40776782)
39. Mourey, L., Re, S. D., Pedelacq, J., Tolstykh, T., Faurie, C., Guillet, V., Stock, J. B., and Samama, J. (2001) Crystal structure of the CheA histidine phosphotransfer domain that mediates response regulator phosphorylation in bacterial chemotaxis J. Biol. Chem. 276 (33) 31074-31082
40. Brunger, A. T. (1992) A System for X-ray Crystallography and NMR. X-PLOR, version 3.1, Yale University Press, New Haven, CT.
41. Zhou, H. and Dahlquist, F. W. (1997) Phosphotransfer site of the chemotaxis-specific protein kinase CheA as revealed by NMR Biochemistry 36 (4) 699-710 (Pubitemid 27110950)
42. Stewart, R. C., Jahreis, K., and Parkinson, J. S. (2000) Rapid phosphotransfer to CheY from a CheA protein lacking the CheY-binding domain Biochemistry 39 (43) 13157-13165
43. Frost, A. A. and Pearson, R. G. (1965) Kinetics and Mechanism, 2nd ed., pp 166, John Wiley & Sons, Inc., New York.
44. Welch, M., Chinardet, N., Mourey, L., Birck, C., and Samama, J. (1998) Structure of the CheY-binding domain of histidine kinase CheA in complex with CheY Nat. Struct. Biol. 5 (1) 25-29 (Pubitemid 28048972)
45. Gouet, P., Chinardet, N., Welch, M., Guillet, V., Cabantous, S., Birck, C., Mourey, L., and Samama, J. (2001) Further insights into the mechanism of function of the response regulator CheY from cystallorgraphic studies of the CheY-CheA124-257 complex Acta Crystallogr. D57, 44-51 (Pubitemid 32062674)
46. Li, J., Swanson, R. V., Simon, M. I., and Weis, R. M. (1995) The response regulators CheB and CheY exhibit competitive binding to the kinase CheA Biochemistry 34 (45) 14626-14636
47. McEvoy, M. M., Muhandiran, D. R., Kay, L. E., and Dahlquist, F. W. (1996) Structure and dynamics of a CheY- binding domain of the chemotaxis kinase CheA determined by nuclear magnetic resonance spectroscopy Biochemistry 35 (18) 5633-5640 (Pubitemid 26143658)
48. Volz, K. and Matsumura, P. (1991) Crystal structure of Escherichia coli CheY refined at 1.7-Å resolution J. Biol. Chem. 266 (23) 15511-15519 (Pubitemid 21907678)
49. Varughese, K. I., Tsigelny, I., and Zhao, H. (2006) The crystal structure of beryllofluoride Spo0F in complex with the phosphotransferase Spo0B represents a phosphotransfer pretransition state J. Bacteriol. 188 (13) 4970-4977 (Pubitemid 43956094)
50. Zhao, X., Copeland, D. M., Soares, A. S., and West, A. H. (2008) Crystal structure of a complex between the phosphorelay protein YPD1 and the response regulator domain of SLN1 bound to a phosphoryl analog J. Mol. Biol. 375 (4) 1141-1151 (Pubitemid 50012875)
51. Park, S., Beel, B. D., Simon, M. I., Bilwes, A. M., and Crane, B. R. (2004) In different organisms, the mode of interaction between two signaling proteins is not necessarily conserved Proc. Natl. Acad. Sci. U.S.A. 101 (32) 11646-11651 (Pubitemid 39095350)