Identification of an anchor residue for CheA-CheY interactions in the chemotaxis system of Escherichia coli

Journal of Bacteriology

Volumn 193, Issue 15, 2011, Pages 3894-3903

  Thakor, Hemang ^a,b   Nicholas, Sarah ^a,c   Porter, Ian M ^a,c   Hand, Nicole ^a   Stewart, Richard C ^a  

^a Bldg 142   (United States)

^b GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CHEA KINASE; CHEY PROTEIN; FUROSEMIDE; MUTANT PROTEIN; YELLOW FLUORESCENT PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CELL ASSAY; CHEMOTAXIS; COMPUTER MODEL; CONTROLLED STUDY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; CHEMOTAXIS; ESCHERICHIA COLI; MEMBRANE PROTEINS; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 79960400935     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00426-11     Document Type: Article

References (73)

1. Ames, P., C. A. Studdert, R. H. Reiser, and J. S. Parkinson. 2002. Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99:7060-7065.
2. Baker, M. D., P. M. Wolanin, and J. B. Stock. 2006. Signal transduction in bacterial chemotaxis. Bioessays 28:9-22.
3. Benedix, A., C. M. Becker, B. L. de Groot, A. Caflisch, and R. A. Bockmann. 2009. Predicting free energy changes using structural ensembles. Nat. Methods 6:3-4.
4. Bilwes, A. M. P., C. M. Quezada, M. Simon, and B. R. Crane. 2003. Structure and function of CheA, the histidine kinase central to bacterial chemotaxis, p. 48-74. In M. Inouye and R. Dutt. (ed.), Histidine kinases in signal transduction. Academic Press, San Diego, CA.
5. Block, S. M., J. E. Segall, and H. C. Berg. 1982. Impulse responses in bacterial chemotaxis. Cell 31:215-226.
6. Bogan, A. A., and K. S. Thorn. 1998. Anatomy of hot spots in protein interfaces. J. Mol. Biol. 280:1-9.
7. Borkovich, K. A., and M. I. Simon. 1990. The dynamics of protein phosphorylation in bacterial chemotaxis. Cell 63:1339-1348.
8. Brissette, P., D. P. Ballou, and V. Massey. 1989. Determination of the dead time of a stopped-flow fluorometer. Anal. Biochem. 181:234-238.
9. Buron-Barral, M., K. K. Gosink, and J. S. Parkinson. 2006. Loss- and gain-of-function mutations in the F1-HAMP region of the Escherichia coli aerotaxis transducer Aer. J. Bacteriol. 188:3477-3486.
10. Clackson, T., and J. A. Wells. 1995. A hot-spot of binding-energy in a hormone-receptor interface. Science 267:383-386.
11. Cluzel, P., M. Surette, and S. Leibler. 2000. An ultrasensitive bacterial motor reveled by monitoring signaling proteins in single cells. Science 287:1652-1655.
12. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
13. Eaton, A. K., and R. C. Stewart. 2009. The two active sites of Thermotoga maritima CheA dimers bind ATP with dramatically different affinities. Biochemistry 48:6412-6422.
14. Fersht, A. 1999. Structure and mechanism in protein science. W. H. Freeman and Co., New York, NY.
15. Hess, J. F., R. B. Bourret, K. Oosawa, P. Matsumura, and M. I. Simon. 1988. Protein phosphorylation and bacterial chemotaxis. Cold Spring Harbor Symp. Quant. Biol. 53:41-48.
16. Hess, J. F., K. Oosawa, N. Kaplan, and M. I. Simon. 1988. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53:79-87.
17. Hirschman, A., M. Boukhvalova, R. VanBruggen, A. J. Wolfe, and R. C. Stewart. 2001. Active site mutations in CheA, the signal-transducing protein kinase of the chemotaxis system in Escherichia coli. Biochemistry 40:13876-13887.
18. Hu, Z. J., B. Y. Ma, H. Wolfson, and R. Nussinov. 2000. Conservation of polar residues as hot spots at protein interfaces. Proteins 39:331-342.
19. Jahreis, K., T. B. Morrison, A. Garzon, and J. S. Parkinson. 2004. Chemotactic signaling by an Escherichia coli CheA mutant that lacks the binding domain for phosphoacceptor partners. J. Bacteriol. 186:2664-2672.
20. Johnson, K. A., Z. B. Simpson, and T. Blom. 2009. Global kinetic explorer: a new computer program for dynamic simulation and fitting of kinetic data. Anal. Biochem. 387:20-29.
21. Kentner, D., and V. Sourjik. 2009. Dynamic map of protein interactions in the Escherichia coli chemotaxis pathway. Mol. Syst. Biol. 5:238.
22. Khan, S., S. Jain, G. P. Reid, and D. R. Trentham. 2004. The fast tumble signal in bacterial chemotaxis. Biophys. J. 86:4049-4058.
23. Kollmann, M., L. Lovdok, K. Bartholome, J. Timmer, and V. Sourjik. 2005. Design principles of a bacterial signalling network. Nature 438:504-507.
24. Krüger, D. M., and H. Gohlke. 2010. DrugScorePPI webserver: fast and accurate in silico alanine scanning for scoring protein-protein interactions. Nucleic Acids Res. 38:W480-W486.
25. Kuzmic, P. 1996. Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase. Anal. Biochem. 237:260-273.
26. Levit, M., Y. Liu, M. Surette, and J. Stock. 1996. Active site interference and asymmetric activation in the chemotaxis protein histidine kinase CheA. J. Biol. Chem. 271:32057-32063.
27. Li, J., R. V. Swanson, M. I. Simon, and R. M. Weis. 1995. The response regulators CheB and CheY exhibit competitive binding to the kinase CheA. Biochemistry 34:14626-14636.
28. Li, M., and G. L. Hazelbauer. 2004. Cellular stoichiometry of the components of the chemotaxis signaling complex. J. Bacteriol. 186:3687-3694.
29. Lise, S., C. Archambeau, M. Pontil, and D. T. Jones. 2009. Prediction of hot spot residues at protein-protein interfaces by combining machine learning and energy-based methods. BMC Bioinformatics 10:365.
30. Liu, J. 1990. Molecular genetics of the chemotaxis signaling pathway in Escherichia coli. Ph.D. thesis. University of Utah, Salt Lake City, UT.
31. Maddock, J. R., and L. Shapiro. 1993. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259:1717-1723.
32. Mayover, T. C., C. J. Halkides, and R. C. Stewart. 1999. Kinetic characterization of CheY phosphorylation reactions: comparison of P-CheA and small-molecule phosphodonors. Biochemistry 38:2259-2271.
33. McEvoy, M. M., A. C. Hausrath, G. B. Randolph, S. J. Remington, and F. W. Dahlquist. 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.
34. Moreira, I. S., P. A. Fernandes, and M. J. Ramos. 2007. Hot spots-a review of the protein-protein interface determinant amino-acid residues. Proteins 68:803-812.
35. Moreira, I. S., P. A. Fernandes, and M. J. Ramos. 2006. Unraveling the importance of protein-protein interaction: application of a computational alanine-scanning mutagenesis to the study of the IgG1 streptococcal protein G (C2 fragment) complex. J. Phys. Chem. B 110:10962-10969.
36. Pons, J., A. Rajpal, and J. F. Kirsch. 1999. Energetic analysis of an antigen/ antibody interface: alanine scanning mutagenesis and double mutant cycles on the hyhel-10/lysozyme interaction. Protein Sci. 8:958-968.
37. Rajamani, D., S. Thiel, S. Vajda, and C. J. Camacho. 2004. Anchor residues in protein-protein interactions. Proc. Natl. Acad. Sci. U. S. A. 101:11287-11292.
38. Raman, S., et al. 2009. Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins 77:89-99.
39. Reichmann, D., et al. 2007. Binding hot spots in the TEM1-BLIP interface in light of its modular architecture. J. Mol. Biol. 365:663-679.
40. Reichmann, D., et al. 2005. The modular architecture of protein-protein binding interfaces. Proc. Natl. Acad. Sci. U. S. A. 102:57-62.
41. Sagi, Y., S. Khan, and M. Eisenbach. 2003. Binding of the chemotaxis response regulator CheY to the isolated, intact switch complex of the bacterial flagellar motor-lack of cooperativity. J. Biol. Chem. 278:25867-25871.
42. Sanders, D. A., B. L. Gillece-Castro, A. M. Stock, A. L. Burlingame, and D. E. Koshland, Jr. 1989. Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J. Biol. Chem. 264:21770-21778.
43. Schreiber, G., and A. R. Fersht. 1993. Interaction of banase with its polypeptide inhibitor barstar studied by protein engineering. Biochemistry 32: 5145-5150.
44. Shaner, N. C., P. A. Steinbach, and R. Y. Tsien. 2005. A guide to choosing fluorescent proteins. Nat. Methods 2:905-909.
45. Shukla, D., and P. Matsumura. 1995. Mutations leading to altered CheA binding cluster on a face of CheY. J. Biol. Chem. 270:24414-24419.
46. Silversmith, R. E., M. D. Levin, E. Schilling, and R. B. Bourret. 2008. Kinetic characterization of catalysis by the chemotaxis phosphatase CheZ. J. Biol. Chem. 283:756-765.
47. Smith, J. G., et al. 2003. Investigation of the role of electrostatic charge in activation of the Escherichia coli response regulator CheY. J. Bacteriol. 185:6385-6391.
48. Sourjik, V. 2004. Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol. 12:569-576.
49. Sourjik, V., and J. P. Armitage. 2010. Spatial organization in bacterial chemotaxis. EMBO J. 29:2724-2733.
50. Sourjik, V., and H. C. Berg. 2000. Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol. Microbiol. 37:740-751.
51. Sourjik, V., and H. C. Berg. 2002. Receptor sensitivity in bacterial chemotaxis. Proc. Natl. Acad. Sci. U. S. A. 99:123-127.
52. Sourjik, V., A. Vaknin, T. S. Shimizu, and H. C. Berg. 2007. In vivo measurement by FRET of pathway activity in bacterial chemotaxis. Methods Enzymol. 423:365-391.
53. Stewart, R. C. 1997. Kinetic characterization of phosphotransfer between CheA and CheY in the bacterial chemotaxis signal transduction pathway. Biochemistry 36:2030-2040.
54. Stewart, R. C., K. Jahreis, and J. S. Parkinson. 2000. Rapid phosphotransfer to CheY from a CheA protein lacking the CheY-binding domain. Biochemistry 39:13157-13165.
55. Stewart, R. C., and R. Van Bruggen. 2004. Association and dissociation kinetics for CheY interacting with the P2 domain of CheA. J. Mol. Biol. 336:287-301.
56. Stewart, R. C., and R. VanBruggen. 2004. Phosphorylation and binding interactions of CheY studies by use of Badan-labeled protein. Biochemistry 43:8766-8777.
57. Swanson, R. V., et al. 1995. Localized perturbations in CheY structure monitored by NMR identify a CheA binding interface. Nat. Struct. Biol. 2:906-910.
58. Szurmant, H., and G. W. Ordal. 2004. Diversity in chemotaxis mechanisms among Bacteria and Archaea. Microbiol. Mol. Biol. Rev. 68:301-319.
59. Thorn, K. S., and A. A. Bogan. 2001. ASEdb: a database of alanine mutations and their effects on the free energy of binding in protein interactions. Bioinformatics 17:284-285.
60. Vaknin, A., and H. C. Berg. 2004. Single-cell FRET imaging of phosphatase activity in the Escherichia coli chemotaxis system. Proc. Natl. Acad. Sci. U. S. A. 101:17072-17077.
61. Vladimirov, N. 2009. Multiscale modeling of bacterial chemotaxis. Ph.D. thesis. Ruperto-Carola University of Heidelberg, Heidelberg, Germany.
62. Vladimirov, N., L. Lovdok, D. Lebiedz, and V. Sourjik. 2008. Dependence of bacterial chemotaxis on gradient shape and adaptation rate. PLoS Comput. Biol. 4:e1000242.
63. Wadhams, G. H., and J. P. Armitage. 2004. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5:1024-1037.
64. Welch, M., N. Chinardet, L. Mourey, C. Birck, and J.-P. Samama. 1998. Structure of the CheY-binding domain of histidine kinase CheA in complex with CheY. Nat. Struct. Biol. 5:25-29.
65. Welch, M., K. Oosawa, S.-I. Aizawa, and M. Eisenbach. 1994. Effects of phosphorylation, Mg2, and conformation of the chemotaxis protein CheY on its binding to the flagellar switch protein FliM. Biochemistry 33:10470-10476.
66. Welch, M., K. Oosawa, S.-I. Aizawa, and M. Eisenbach. 1993. Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc. Natl. Acad. Sci. U. S. A. 90:8787-8791.
67. Wolfe, A. J., and H. C. Berg. 1989. Migration of bacteria in semisolid agar. Proc. Natl. Acad. Sci. U. S. A. 86:6973-6977.
68. Wright, S., B. Walia, J. S. Parkinson, and S. Khan. 2006. Differential activation of Escherichia coli chemoreceptors by blue-light stimuli. J. Bacteriol. 188:3962-3971.
69. Yen, K. M. 1991. Construction of cloning cartridges for development of expression vectors in gram-negative bacteria. J. Bacteriol. 173:5328-5335.
70. Zacharias, D. A., J. D. Violin, A. C. Newton, and R. Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913-916.
71. Zhang, P. J., C. M. Khursigara, L. M. Hartnell, and S. Subramaniam. 2007. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 104:3777-3781.
72. Zhou, H., and F. W. Dahlquist. 1997. Phosphotransfer site of the chemotaxisspecific protein kinase CheA as revealed by NMR. Biochemistry 36:699-710.
73. Zhou, H. J., et al. 1996. Phosphotransfer and CheY-binding domains of the histidine autokinase CheA are joined by a flexible linker. Biochemistry 35:433-443.