Structure of a conserved receptor domain that regulates kinase activity: The cytoplasmic domain of bacterial taxis receptors

Current Opinion in Structural Biology

Volumn 10, Issue 4, 2000, Pages 462-469

  Falke, Joseph J ^a   Kim, Sung Hou ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYTOPLASM PROTEIN; MEMBRANE RECEPTOR; PHOSPHOTRANSFERASE; RECEPTOR PROTEIN;

BACTERIUM; CELL MOTILITY; COVALENT BOND; CRYSTALLOGRAPHY; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

EID: 0033931244     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(00)00115-9     Document Type: Review

References (69)

1. Kim K.K., Yokota H., Kim S.H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature. 400:1999;787-792. The authors describe the crystal structure of the isolated serine receptor cytoplasmic domain, providing the first high-resolution view of this conserved signaling motif, particularly the functionally critical signaling subdomain.
2. Bass R.B., Falke J.J. The aspartate receptor cytoplasmic domain: in situ chemical analysis of structure, mechanism and dynamics. Structure. 7:1999;829-840. The chemically derived structure of the dimeric aspartate receptor cytoplasmic domain reveals architectural, dynamical and functional features of the four-helix bundle in the full-length, membrane-bound receptor.
3. Armitage J.P. Bacterial tactic responses. Adv Microb Physiol. 41:1999;229-289.
4. Falke J.J., Bass R.B., Butler S.L., Chervitz S.A., Danielson M.A. 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. 13:1997;457-512.
5. Stock J.B., Surette M. Chemotaxis. Neidhardt R.C. Escherichia Coli and Salmonella Typhimurium: Cellular and Molecular Biology, edn 2. 1996;123-145 ASM Press, Washington, DC.
6. Blair D.F. How bacteria sense and swim. Annu Rev Microbiol. 49:1995;489-522.
7. Mowbray S.L. Chemotaxis receptors: a progress report on structure and function. J Struct Biol. 124:1998;257-275.
8. Le Moual H., Koshland D.E. Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis. J Mol Biol. 261:1996;568-585.
9. Schultz J., Copley R.R., Doerks T., Ponting C.P., Bork P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 28:2000;231-234.
10. Danielson, M.A.: Molecular mechanism of transmembrane signaling and kinase regulation by the aspartate receptor of bacterial chemotaxis [PhD Thesis]. Boulder, CO: University of Colorado; 1997.
11. Hoff W.D., Jung K.H., Spudich J.L. Molecular mechanism of photosignaling by archaeal sensory rhodopsins. Annu Rev Biophys Biomol Struct. 26:1997;223-258.
12. Bibikov S.I., Biran R., Rudd K.E., Parkinson J.S. A signal transducer for aerotaxis in Escherichia coli. J Bacteriol. 179:1997;4075-4079.
13. Rebbapragada A., Johnson M.S., Harding G.P., Zuccarelli A.J., Fletcher H.M., Zhulin I.B., Taylor B.L. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc Natl Acad Sci USA. 94:1997;10541-10546.
14. Brooun A., Zhang W.S., Alam M. Primary structure and functional analysis of the soluble transducer protein HtrXI in the archaeon Halobacterium salinarium. J Bacteriol. 179:1997;2963-2968.
15. Milburn M.V., Prive G.G., Milligan D.L., Scott W.G., Yeh J., Jancarik J., Koshland D.E., Kim S.H. Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science. 254:1991;1342-1347.
16. Yeh J.I., Biemann H.P., Pandit J., Koshland D.E., Kim S.H. The three-dimensional structure of the ligand binding domain of a wild type bacterial chemotaxis receptor: structural comparison to the cross-linked mutant forms and conformational changes upon ligand binding. J Biol Chem. 268:1993;9787-9792.
17. Bowie J.U., Pakula A.A., Simon M.I. The three-dimensional structure of the aspartate receptor from Escherichia coli. Acta Crystallogr. 51:1995;145-154.
18. Yeh J.I., Biemann H.P., Prive G.G., Pandit J., Koshland D.E., Kim S.H. High resolution structures of the ligand binding domain of the wild type bacterial aspartate receptor. J Mol Biol. 262:1996;186-201.
19. Chi Y.I., Yokota H., Kim S.H. Apo structure of the ligand-binding domain of aspartate receptor from Escherichia coli and its comparison with ligand-bound or pseudoligand-bound structures. FEBS Lett. 414:1997;327-332.
20. Falke J.J., Dernburg A.F., Sternburg D.A., Zalkin N., Milligan D.L., Koshland D.E. Structure of a bacterial sensory receptor: a site directed sulfhydryl study. J Biol Chem. 263:1988;14850-14858.
21. Chervitz S.A., Lin C.M., Falke J.J. Transmembrane signaling by the aspartate receptor: engineered disulfides reveal static regions of the subunit interface. Biochemistry. 34:1995;9722-9733.
22. Chervitz S.A., Falke J.J. Lock on/off disulfides identify the transmembrane signaling helix of the aspartate receptor. J Biol Chem. 270:1995;24043-24053.
23. Chervitz S.A., Falke J.J. Molecular mechanism of transmembrane signaling by the aspartate receptor: a model. Proc Natl Acad Sci USA. 93:1996;2545-2550.
24. Lee G.F., Burrows G.G., Lebert M.R., Dutton D.P., Hazelbauer G.L. Deducing the organization of a transmembrane domain by disulfide cross-linking: the bacterial chemoreceptor Trg. J Biol Chem. 269:1994;29920-29927.
25. Lee G.F., Hazelbauer G.L. Quantitative approaches to utilizing mutational analysis and disulfide cross-linking for modeling a transmembrane domain. Protein Sci. 4:1995;1100-1107.
26. Hughson A.G., Hazelbauer G.L. Detecting the conformational change of transmembrane signaling in a bacterial chemoreceptor by measuring effects on disulfide cross- linking in vivo. Proc Natl Acad Sci USA. 93:1996;11546-11551.
27. Hughson A.G., Lee G.F., Hazelbauer G.L. Analysis of protein structure in intact cells: crosslinking in vivo between introduced cysteines in the transmembrane domain of a bacterial chemoreceptor. Protein Sci. 6:1997;315-322.
28. Krikos A., Conley M.P., Boyd A., Berg H.C., Simon M.I. Chimeric chemosensory transducers of E. coli. Proc Natl Acad Sci USA. 82:1985;1326-1330.
29. Baumgartner J.W., Kim C., Brissette R.E., Inouye M., Park C., Hazelbauer G.L. Transmembrane signaling 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. 176:1994;1157-1163.
30. Tatsuno I., Lee L., Kawagishi I., Homma M., Imae Y. Transmembrane signaling by the chimeric chemosensory receptors of E. coli Tsr and Tar with heterologous membrane-spanning regions. Mol Microbiol. 14:1994;755-762.
31. Zhang X.N., Zhu J.Y., Spudich J.L. The specificity of interaction of archaeal transducers with their cognate sensory rhodopsins is determined by their transmembrane helices. Proc Natl Acad Sci USA. 96:1999;857-862.
32. Mowbray S.L., Foster D.L., Koshland D.E. Proteolytic fragments identified with domains of the aspartate chemoreceptor. J Biol Chem. 260:1985;11711-11718.
33. Long D.G., Weis R.M. Oligomerization of the cytoplasmic fragment from the aspartate receptor of Escherichia coli. Biochemistry. 31:1992;9904-9911.
34. Seeley S.K., Weis R.M., Thompson L.K. The cytoplasmic fragment of the aspartate receptor displays globally dynamic behavior. Biochemistry. 35:1996;5199-5206.
35. Stock J.B., Lukat G.S., Stock A.M. Bacterial chemotaxis and the molecular logic of intracellular signal transduction networks. Annu Rev Biophys Chem. 20:1991;109-136.
36. Ames P., Yu Y.A., Parkinson J.S. Methylation segments are not required for chemotactic signaling by cytoplasmic fragments of Tsr, the methyl-accepting serine chemoreceptor of E. coli. Mol Microbiol. 19:1996;737-746.
37. Ames P., Parkinson J.S. Constitutively signaling fragments of Tsr, the E. coli serine chemoreceptor. J Bacteriol. 176:1994;6340-6348.
38. Surette M.G., Stock J.B. Role of alpha-helical coiled-coil interactions in receptor dimerization, signaling, and adaptation during bacterial chemotaxis. J Biol Chem. 271:1996;17966-17973.
39. Cochran A.G., Kim P.S. Imitation of E. coli aspartate receptor signaling in engineered dimers of the cytoplasmic domain. Science. 271:1996;1113-1116.
40. Singh M., Berger B., Kim P.S., Berger J.M., Cochran A.G. Computational learning reveals coiled coil-like motifs in histidine kinase linker domains. Proc Natl Acad Sci USA. 95:1998;2738-2743.
41. Aravind L., Ponting C.P. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett. 176:1999;111-116. This paper defines the conserved HAMP domain shared by various signaling proteins, including the linker regions of methyl-accepting taxis proteins.
42. Williams S.B., Stewart V. Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction. Mol Microbiol. 33:1999;1093-1102.
43. Danielson M.A., Bass R.B., Falke J.J. Cysteine and disulfide scanning reveals a regulatory alpha-helix in the cytoplasmic domain of the aspartate receptor. J Biol Chem. 272:1997;32878-32888.
44. Butler S.L., Falke J.J. Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor. Biochemistry. 37:1998;10746-10756.
45. Bass R.B., Falke J.J. Detection of a conserved alpha-helix in the kinase-docking region of the aspartate receptor by cysteine and disulfide scanning. J Biol Chem. 273:1998;25006-25014.
46. Bass R.B., Coleman M.D., Falke J.J. Signaling domain of the aspartate receptor is a helical hairpin with a localized kinase docking surface: cysteine and disulfide scanning studies. Biochemistry. 38:1999;9317-9327. Chemical evidence reveals the dimerization of two helical hairpins, one from each subunit of the dimer, to form a four-helix bundle in the cytoplasmic domain of the membrane-bound aspartate receptor.
47. Falke J.J., Sternberg D.W., Koshland D.E. Site-directed chemistry and spectroscopy: applications in the aspartate receptor system. Biophys J. 49:1986;20.
48. Falke J.J., Koshland D.E. Global flexibility in a sensory receptor: a site directed disulfide approach. Science. 237:1987;1596-1600.
49. Careaga C.L., Falke J.J. Thermal motions of surface alpha-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping. J Mol Biol. 226:1992;1219-1235.
50. Sahin-Toth M., Kaback H.R. Cysteine scanning mutagenesis of putative transmembrane helices IX and X in the lactose permease of Escherichia coli. Protein Sci. 2:1993;1024-1033.
51. Kim S.H. Frozen dynamic dimer model for transmembrane signaling in bacterial chemotaxis receptors. Protein Sci. 3:1994;159-165.
52. Long D.G., Weis R.M. Oligomerization of the cytoplasmic fragment from the aspartate receptor of E. coli. Biochemistry. 31:1992;9904-9911.
53. Maddock J.R., Shapiro L. Polar location of the chemoreceptor complex in the E. coli cell. Science. 259:1993;1717-1723.
54. Skidmore J.M., Ellefson D.D., McNamara B.P., Couto M.M.P., Wolfe A.J., Maddock J.R. Polar clustering of the chemoreceptor complex in E. coli occurs in the absence of complete CheA function. J Bacteriol. 182:2000;967-973.
55. Stock J., Levit N. Signal transduction: hair brains in bacterial chemotaxis. Curr Biol. 10:2000;11-14. A recent summary of evidence that the cytoplasmic domain of the E. coli chemoreceptor may form higher order oligomers in vitro and in vivo.
56. Tatsuno I., Homma M., Oosawa K., Kawagishi I. Signaling by the E. coli aspartate chemoreceptor Tar with a single cytoplasmic domain per dimer. Science. 274:1996;423-425.
57. Gardina P.J., Manson M.D. Attractant signaling by an aspartate chemoreceptor dimer with a single cytoplasmic domain. Science. 274:1996;425-426.
58. Nishiyama S., Umemura T., Nara T., Homma M., Kawagishi I. Conversion of a bacterial warm sensor to a cold sensor by methylation of a single residue in the presence of an attractant. Mol Microbiol. 32:1999;357-365.
59. Trammell M.A., Falke J.J. Identification of a site critical for kinase regulation on the central processing unit (CPU) helix of the aspartate receptor. Biochemistry. 38:1999;329-336. Evidence that a region of the subunit interface within the aspartate receptor cytoplasmic domain is tightly coupled to kinase regulation is presented.
60. Liu J.D., Parkinson J.S. Genetic-evidence for interaction between the Chew and Tsr proteins during chemoreceptor signaling by E. coli. J Bacteriol. 173:1991;4941-4951.
61. Bilwes A.M., Alex L.A., Crane B.R., Simon M.I. Structure of CheA, a signal-transducing histidine kinase. Cell. 96:1999;131-141. The authors describe the crystal structure of the catalytic and dimerization domains of CheA, the histidine kinase regulated by the serine and aspartate receptor cytoplasmic domains.
62. Zhou H.J., Dahlquist F.W. Phosphotransfer site of the chemotaxis-specific protein kinase CheA as revealed by NMR. Biochemistry. 36:1997;699-710.
63. McEvoy M.M., Muhandiram D.R., Kay L.E., Dahlquist F.W. Structure and dynamics of a CheY-binding domain of the chemotaxis kinase CheA determined by nuclear-magnetic-resonance spectroscopy. Biochemistry. 35:1996;5633-5640.
64. Djordjevic S., Stock A.M. Structural analysis of bacterial chemotaxis proteins: components of a dynamic signaling system. J Struct Biol. 124:1998;189-200.
65. Li G.Y., Weis R.M. Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of E. coli. Cell. 100:2000;357-365. Positive cooperativity in ligand-induced kinase regulation suggests that two or more serine receptor dimers may interact in cooperative oligomers.
66. Bornhorst J.A., Falke J.J. Attractant regulation of the aspartate receptor-kinase complex: limited cooperative interactions between receptors and effects of receptor modification state. Biochemistry. 2000;. in press. Ligand-induced kinase regulation exhibits limited positive cooperativity between a small number of aspartate receptor dimers.
67. Wu J.G., Li J.Y., Li G.Y., Long D.G., Weis R.M. The receptor-binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry. 35:1996;4984-4993.
68. Li J.Y., Li G.Y., Weis R.M. The serine chemoreceptor from E. coli is methylated through an inter-dimer process. Biochemistry. 36:1997;11851-11857.
69. Le Moual H., Quang T., Koshland D.E. Methylation of the E. coli chemotaxis receptors: intra- and interdimer mechanisms. Biochemistry. 36:1997;13441-13448.