Evidence that the adaptation region of the aspartate receptor is a dynamic four-helix bundle: Cysteine and bisulfide scanning studies

Biochemistry

Volumn 44, Issue 38, 2005, Pages 12655-12666

  Winston, Susanna E ^a   Mehan, Ryan ^a   Falke, Joseph J ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; MAPPING; SIGNALING;

CHEMOTAXIS; CYSTEINES; KINASE; THERMAL DYNAMICS;

CELLS;

ASPARTATE RECEPTOR; CHEA KINASE; CYSTEINE; DISULFIDE; RECEPTOR; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ADAPTATION; ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMORECEPTOR; CHEMOTAXIS; COMPLEX FORMATION; CONTROLLED STUDY; DISULFIDE BOND; ENZYME REGULATION; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; CYSTEINE; DISULFIDES; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, AMINO ACID;

ESCHERICHIA COLI; SALMONELLA TYPHIMURIUM;

EID: 25444437722     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0507884     Document Type: Article

References (73)

1. Swanson, R. V., Alex, L. A., and Simon, M. I. (1994) Histidine and aspartate phosphorylation: Two-component systems and the limits of homology, Trends Biochem. Sci. 19, 485-490.
2. Parkinson, J. S. (1993) Signal transduction schemes of bacteria. Cell 73, 857-871.
3. Spudich, J. L., and Luecke, H. (2002) Sensory rhodopsin II: Functional insights from structure, Curr. Opin. Struct. Biol. 12, 540-546.
4. Falke, J. J., and Hazelbauer, G. L. (2001) Transmembrane signaling in bacterial chemoreceptors, Trends Biochem. Sci. 26, 257-265.
5. Falke, J. J., Bass, R. B., Butler, S. L., Chervitz, S. A., and Danielson, M. A. (1997) The two-component signaling pathway of bacterial chemotaxis: A molecular view of signal transduction by receptors, kinases, and adaptation enzymes, Annu. Rev. Cell Dev. Biol. 13, 457-512.
6. Zhulin, I. B., Nikolskaya, A. N., and Galperin, M. Y. (2003) Common extracellular sensory domains in transmembrane receptors for diverse signal transduction pathways in bacteria and archaea, J. Bacteriol. 185, 285-294.
7. Le Moual, H., and Koshland, D. E., Jr. (1996) Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis, J. Mol. Biol. 261, 568-585.
8. Danielson, M. A. (1997) in Department of Chemistry and Biochemistry, pp 142, University of Colorado, Boulder, CO.
9. Trivedi, V. D., and Spudich, J. L. (2003) Photostimulation of a sensory rhodopsin II/HtrII/Tsr fusion chimera activates CheA-autophosphorylation and CheY-phosphotransfer in vitro, Biochemistry 42, 13887-13892.
10. Baumgartner, J. W., Kim, C., Brissette, R. E., Inouye, M., Park, C., and Hazelbauer, G. L. (1994) Transmembrane signalling by a hybrid protein: Communication from the domain of chemoreceptor Trg that recognizes sugar-binding proteins to the kinase/phosphatase domain of osmosensor EnvZ, J. Bacteriol. 176, 1157-1163.
11. Krikos, A., Conley, M. P., Boyd, A., Berg, H. C., and Simon, M. I. (1985) Chimeric chemosensory transducers of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 82, 1326-1330.
12. Utsumi, R., Brissette, R. E., Rampersaud, A., Forst, S. A., Oosawa, K., and Inouye, M. (1989) Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate, Science 245, 1246-1249.
13. Moe, G. R., Bollag, G. E., and Koshland, D. E., Jr. (1989) Transmembrane signaling by a chimera of the Escherichia coli aspartate receptor and the human insulin receptor, Proc. Natl. Acad. Sci. U.S.A. 86, 5683-5687.
14. Biemann, H. P., Harmer, S. L., and Koshland, D. E., Jr. (1996) An aspartate/insulin receptor chimera mitogenically activates fibroblasts, J. Biol. Chem. 271, 27927-27930.
15. Segall, J. E., Block, S. M., and Berg, H. C. (1986) Temporal comparisons in bacterial chemotaxis, Proc. Natl. Acad. Sci. U.S.A. 83, 8987-8991.
16. 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.
17. Schuster, S. C., Swanson, R. V., Alex, L. A., Bourret, R. B., and Simon, M. I. (1993) Assembly and function of a quaternary signal transduction complex monitored by surface plasmon resonance, Nature 365, 343-347.
18. Wang, H., and Matsumura, P. (1997) Phosphorylating and dephosphorylating protein complexes in bacterial chemotaxis, J. Bacteriol. 179, 287-289.
19. Bourret, R. B., Borkovich, K. A., and Simon, M. I. (1991) Signal transduction pathways involving protein phosphorylation in prokaryotes, Annu. Rev. Biochem. 60, 401-441.
20. 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.
21. Kojima, S., and Blair, D. F. (2004) The bacterial flagellar motor: Structure and function of a complex molecular machine, Int. Rev. Cytol. 233, 93-134.
22. Bren, A., and Eisenbach, M. (2000) How signals are heard during bacterial chemotaxis: Protein-protein interactions in sensory signal propagation, J. Bacteriol. 182, 6865-6873.
23. Bowie, J. U., Pakula, A. A., and Simon, M. I. (1995) The three-dimensional structure of the aspartate receptor from Escherichia coli, Acta Crystallogr., Sect. D: Biol. Crystallogr. 51, 145-154.
24. Milburn, M. V., Prive, 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.
25. Pakula, A. A., and Simon, M. I. (1992) Determination of transmembrane protein structure by disulfide cross-linking: The Escherichia coli Tar receptor, Proc. Natl. Acad. Sci. U.S.A. 89, 4144-4148.
26. Chervitz, S. A., and Falke, J. J. (1996) Molecular mechanism of transmembrane signaling by the aspartate receptor: A model, Proc. Natl. Acad. Sci. U.S.A. 93, 2545-2550.
27. Chervitz, S. A., and Falke, J. J. (1995) Lock on/off disulfides identify the transmembrane signaling helix of the aspartate receptor, J. Biol. Chem. 270, 24043-24053.
28. Hughson, A. G., and Hazelbauer, G. L. (1996) Detecting the conformational change of transmembrane signaling in a bacterial chemoreceptor by measuring effects on disulfide cross-linking in vivo, Proc. Natl. Acad. Sci. U.S.A. 93, 11546-11551.
29. Ottemann, K. M., Xiao, W., Shin, Y. K., and Koshland, D. E., Jr. (1999) A piston model for transmembrane signaling of the aspartate receptor [see comments], Science 285, 1751-1754.
30. Isaac, B., Gallagher, G. J., Balazs, Y. S., and Thompson, L. K. (2002) Site-directed rotational resonance solid-state NMR distance measurements probe structure and mechanism in the transmembrane domain of the serine bacterial chemoreceptor, Biochemistry 41, 3025-3036.
31. Draheim, R. R., Bormans, A. F., Lai, R. Z., and Manson, M. D, (2005) Tryptophan residues flanking the second transmembrane helix (TM2) set the signaling state of the Tar chemoreceptor, Biochemistry 44, 1268-1277.
32. Gardina, P. J., Bormans, A. F., and Manson, M. D. (1998) A mechanism for simultaneous sensing of aspartate and maltose by the Tar chemoreceptor of Escherichia coli, Mol. Microbiol. 29, 1147-1154.
33. Miller, A. S., and Falke, J. J. (2004) Side chains at the membrane-water interface modulate the signaling state of a transmembrane receptor, Biochemistry 43, 1763-1770.
34. Ames, P., and Parkinson, J. S. (1994) Constitutively signaling fragments of Tsr, the Escherichia coli serine chemoreceptor, J. Bacteriol. 176, 6340-6348.
35. Bass, R. B., Coleman, M. D., and Falke, J. J. (1999) Signaling domain of the aspartate receptor is a helical hairpin with a localized kinase docking surface: Cysteine and disulfide scanning studies, Biochemistry 38, 9317-9327.
36. Shiomi, D., Zhulin, I. B., Homma, M., and Kawagishi, I. (2002) Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase, J. Biol. Chem. 277, 42325-42333.
37. Blair, D. F. (1995) How bacteria sense and swim, Annu. Rev. Microbiol. 49, 489-522.
38. Nishiyama, S. I., Umemura, T., Nara, T., Homma, M., and Kawagishi, I. (1999) Conversion of a bacterial warm sensor to a cold sensor by methylation of a single residue in the presence of an attractant, Mol. Microbiol. 32, 357-365.
39. 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.
40. Falke, J. J., and Kim, S. H. (2000) Structure of a conserved receptor domain that regulates kinase activity: The cytoplasmic domain of bacterial taxis receptors, Curr. Opin. Struct. Biol. 10, 462-469.
41. Bass, R. B., and Falke, J. J. (1999) The aspartate receptor cytoplasmic domain: In situ chemical analysis of structure, mechanism, and dynamics, Struct. Fold Des. 7, 829-840.
42. Studdert, C. A., and Parkinson, J. S. (2004) Crosslinking snapshots of bacterial chemoreceptor squads, Proc. Natl. Acad. Sci. U.S.A. 101, 2117-2122.
43. Ames, P., Studdert, C. A., Reiser, R. H., and Parkinson, J. S. (2002) Collaborative signaling by mixed chemoreceptor teams in Escherichia coll, Proc. Natl. Acad. Sci. U.S.A. 99, 7060-7065.
44. Bornhorst, J. A., and Falke, J. J. (2000) Attractant regulation of the aspartate receptor-kinase complex: Limited cooperative interactions between receptors and effects of the receptor modification state, Biochemistry 39, 9486-9493.
45. Li, G., and Weis, R. M. (2000) Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli, Cell 100, 357-365.
46. Sourjik, V., and Berg, H. C. (2004) Functional interactions between receptors in bacterial chemotaxis, Nature 428, 437-441.
47. Seeley, S. K., Weis, R. M., and Thompson, L. K. (1996) The cytoplasmic fragment of the aspartate receptor displays globally dynamic behavior, Biochemistry 35, 5199-5206.
48. Murphy, O. J., III, Yi, X., Weis, R. M., and Thompson, L. K. (2001) Hydrogen exchange reveals a stable and expandable core within the aspartate receptor cytoplasmic domain, J. Biol. Chem. 276, 43262-43269.
49. Danielson, M. A., Bass, R. B., and Falke, J. J. (1997) Cysteine and disulfide scanning reveals a regulatory α-helix in the cytoplasmic domain of the aspartate receptor, J. Biol. Chem. 272, 32878-32888.
50. Long, D. G., and Weis, R. M. (1992) Oligomerization of the cytoplasmic fragment from the aspartate receptor of Escherichia coli, Biochemistry 31, 9904-9911.
51. Foster, D. L., Mowbray, S. L., Jap, B. K., and Koshland, D. E., Jr. (1985) Purification and characterization of the aspartate chemoreceptor, J. Biol. Chem. 260, 11706-11710.
52. Falke, J. J., Sternberg, D. E., and Koshland, D. E., Jr. (1986) Site-directed sulfhydryl chemistry and spectroscopy: Applications in the aspartate receptor system, Biophys. J. 49, 20a.
53. Falke, J. J., and Koshland, D. E., Jr. (1987) Global flexibility in a sensory receptor: A site-directed cross-linking approach, Science 237, 1596-1600.
54. Butler, S. L., and Falke, J. J. (1998) Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor, Biochemistry 37, 10746-10756.
55. Hughson, A. G., Lee, G. F., and Hazelbauer, G. L. (1997) Analysis of protein structure in intact cells: Crosslinking in vivo between introduced cysteines in the transmembrane domain of a bacterial chemoreceptor, Protein Sci. 6, 315-322.
56. Kaback, H. R., Sahin-Toth, M., and Weinglass, A. B. (2001) The kamikaze approach to membrane transport, Nat. Rev. Mol. Cell Biol. 2, 610-620.
57. Liu, J. D., and Parkinson, J. S. (1989) Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis, Proc. Natl. Acad. Sci. U.S.A. 86. 8703-8707.
58. Chervitz, S. A., Lin, C. M., and Falke, J. J. (1995) Transmembrane signaling by the aspartate receptor: Engineered disulfides reveal static regions of the subunit interface, Biochemistry 34, 9722-9733.
59. Kunkel, T. A., Bebenek, K., and McClary, J. (1991) Efficient site-directed mutagenesis using uracil-containing DNA, Methods Enzymol. 204, 125-139.
60. Adler, J. (1966) Bacterial chemotaxis, Science 153, 708-716.
61. 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.
62. Clarke, S., and Koshland, D. E., Jr. (1979) Membrane receptors for aspartate and serine in bacterial chemotaxis, J. Biol. Chem. 254, 9695-9702.
63. Bass, R. B., and Falke, J. J. (1998) Detection of a conserved α-helix in the kinase-docking region of the aspartate receptor by cysteine and disulfide scanning, J. Biol. Chem, 273, 25006-25014.
64. Shapiro, M. J., and Koshland, D. E., Jr. (1994) Mutagenic studies of the interaction between the aspartate receptor and methyltransferase from Escherichia coli, J. Biol. Chem. 269, 11054-11059.
65. Bornhorst, J. A., and Falke, J. J. (2003) Quantitative analysis of aspartate receptor signaling complex reveals that the homogeneous two-state model is inadequate: Development of a heterogeneous two-state model, J. Mol. Biol. 326, 1597-1614.
66. Careaga, C. L., and Falke, J. J. (1992) Thermal motions of surface α-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping, J. Mol. Biol. 276, 1219-1235.
67. Kim, S. H. (1994) "Frozen" dynamic dimer model for transmembrane signaling in bacterial chemotaxis receptors. Protein Sci. 3, 159-165.
68. Kim, S. H., Wang, W., and Kim, K. K. (2002) Dynamic and clustering model of bacterial chemotaxis receptors: Structural basis for signaling and high sensitivity, Proc. Natl. Acad. Sci. U.S.A. 99, 11611-11615.
69. Starrett, D. J., and Falke, J. J. (2005) Adaptation mechanism of the aspartate receptor: Electrostatics of the adaptation subdomain play a key role in modulating kinase activity, Biochemistry, in press.
70. Tatsuno, I., Homma, M., Oosawa, K., and Kawagishi, I. (1996) Signaling by the Escherichia coli aspartate chemoreceptor Tar with a single cytoplasmic domain per dimer, Science 274, 423-425.
71. Gardina, P. J., and Manson, M. D. (1996) Attractant signaling by an aspartate chemoreceptor dimer with a single cytoplasmic domain, Science 274, 425-426.
72. Lefman, J., Zhang, P., Hirai, T., Weis, R. M., Juliani, J., Bliss, D., Kessel, M., Bos, E., Peters, P. J., and Subramaniam, S. (2004) Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr, J. Bacterial. 186, 5052-5061.
73. Chothia, C., and Lesk, A. M. (1985) Helix movements in proteins, Trends Biochem. Sci. 10, 116-118.