Mutational analysis of the connector segment in the HAMP domain of Tsr, the Escherichia coli serine chemoreceptor

Journal of Bacteriology

Volumn 190, Issue 20, 2008, Pages 6676-6685

  Ames, Peter ^a   Zhou, Qin ^a   Parkinson, John S ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; GLYCINE; MUTANT PROTEIN; PHOSPHOTRANSFERASE; SERINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CHEMORECEPTOR; CONFORMATION; ESCHERICHIA COLI; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; THERMOPHILIC BACTERIUM;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CHEMOTAXIS; DNA MUTATIONAL ANALYSIS; ESCHERICHIA COLI; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, INSERTIONAL; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 53849112614     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00750-08     Document Type: Article

References (49)

1. Alexander, R. P., and I. B. Zhulin. 2007. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc. Natl. Acad. Sci. USA 104:2885-2890.
2. Ames, P., and J. S. Parkinson. 2006. Conformational suppression of inter-receptor signaling defects. Proc. Natl. Acad. Sci. USA 103:9292-9297.
3. Ames, P., and J. S. Parkinson. 1994. Constitutively signaling fragments of Tsr, the Escherichia coli serine chemoreceptor. J. Bacteriol. 176:6340-6348.
4. Ames, P., and J. S. Parkinson. 1988. Transmembrane signaling by bacterial chemoreceptors: E. coli transducers with locked signal output. Cell 55:817-826.
5. 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. USA 99:7060-7065.
6. Appleman, J. A., L. L. Chen, and V. Stewart. 2003. Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases. J. Bacteriol. 185:4872-4882.
7. Appleman, J. A., and V. Stewart. 2003. Mutational analysis of a conserved signal-transducing element: the HAMP linker of the Escherichia coli nitrate sensor NarX. J. Bacteriol. 185:89-97.
8. Aravind, L., and C. P. Ponting. 1999. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol. Lett. 176:111-116.
9. Baumgartner, J. W., C. Kim, R. R. Brissette, M. Inouye, C. Park, and G. L. Hazelbauer. 1994. Transmembrane signalling by a hybrid protein: communication from the domain of chemoreceptor Trg that recognizes sugarbinding proteins to kinase/phosphatase domain of osmosensor EnvZ. J. Bacteriol. 176:1157-1163.
10. Bibikov, S. I., A. C. Miller, K. K. Gosink, and J. S. Parkinson. 2004. Methylation-independent aerotaxis mediated by the Escherichia coli Aer protein. J. Bacteriol. 186:3730-3737.
11. Boldog, T., S. Grimme, M. Li, S. G. Sligar, and G. L. Hazelbauer. 2006. Nanodiscs separate chemoreceptor oligomeric states and reveal their signaling properties. Proc. Natl. Acad. Sci. USA 103:11509-11514.
12. Bolivar, F., R. Rodriguez, P. J. Greene, M. C. Betlach, H. L. Heyneker, and H. W. Boyer. 1977. Construction and characterization of new cloning vehicles. Gene 2:95-113.
13. Bornhorst, J. A., and J. J. Falke. 2001. Evidence that both ligand binding and covalent adaptation drive a two-state equilibrium in the aspartate receptor signaling complex. J. Gen. Physiol. 118:693-710.
14. 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.
15. Butler, S. L., and J. J. Falke. 1998. Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor. Biochem. 37:10746-10756.
16. Chang, A. C. Y., and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the p15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
17. Cochran, A. G., and P. S. Kim. 1996. Imitation of Escherichia coli aspartate receptor signaling in engineered dimers of the cytoplasmic domain. Science 271:1113-1116.
18. Falke, J. J., and G. L. Hazelbauer. 2001. Transmembrane signaling in bacterial chemoreceptors. Trends Biochem. Sci. 26:257-265.
19. Francis, N. R., M. N. Levit, T. R. Shaikh, L. A. Melanson, J. B. Stock, and D. J. DeRosier. 2002. Subunit organization in a soluble complex of Tar, CheW, and CheA by electron microscopy. J. Biol. Chem. 277:36755-36759.
20. Francis, N. R., P. M. Wolanin, J. B. Stock, D. J. Derosier, and D. R. Thomas. 2004. Three-dimensional structure and organization of a receptor/signaling complex. Proc. Natl. Acad. Sci. USA 101:17480-17485.
21. Gosink, K. K., M. Buron-Barral, and J. S. Parkinson. 2006. Signaling interactions between the aerotaxis transducer Aer and heterologous chemoreceptors in Escherichia coli. J. Bacteriol. 188:3487-3493.
22. Greer-Phillips, S. E., G. Alexandre, B. L. Taylor, and I. B. Zhulin. 2003. Aer and Tsr guide Escherichia coli in spatial gradients of oxidizable substrates. Microbiology 149:2661-2667.
23. Hazelbauer, G. L., J. J. Falke, and J. S. Parkinson. 2008. Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem. Sci. 33:9-19.
24. Hulko, M., F. Berndt, M. Gruber, J. U. Linder, V. Truffault, A. Schultz, J. Martin, J. E. Schultz, A. N. Lupas, and M. Coles. 2006. The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929-940.
25. Jung, K. H., E. N. Spudich, V. D. Trivedi, and J. L. Spudich. 2001. An archaeal photosignal-transducing module mediates phototaxis in Escherichia coli. J. Bacteriol. 183:6365-6371.
26. Kalman, L. V., and R. P. Gunsalus. 1990. Nitrate- and molybdenum-independent signal transduction mutations in narX that alter regulation of anaerobic respiratory genes in Escherichia coli. J. Bacteriol. 172:7049-7056.
27. Kristich, C. J., and G. W. Ordal. 2004. Analysis of chimeric chemoreceptors in Bacillus subtilis reveals a role for CheD in the function of the McpC HAMP domain. J. Bacteriol. 186:5950-5955.
28. Lai, W. C., B. D. Beel, and G. L. Hazelbauer. 2006. Adaptational modification and ligand occupancy have opposite effects on positioning of the transmembrane signalling helix of a chemoreceptor. Mol. Microbiol. 61:1081-1090.
29. Liu, J. D., and J. S. Parkinson. 1989. Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 86:8703-8707.
30. Ma, Q., M. S. Johnson, and B. L. Taylor. 2005. Genetic analysis of the HAMP domain of the Aer aerotaxis sensor localizes flavin adenine dinucleotide-binding determinants to the AS-2 helix. J. Bacteriol. 187:193-201.
31. Montefusco, D. J., A. L. Shrout, T. Y. Besschetnova, and R. M. Weis. 2007. Formation and activity of template-assembled receptor signaling complexes. Langmuir 23:3280-3289.
32. Parkinson, J. S. 1976. cheA, cheB, and cheC genes of Escherichia coli and their role in chemotaxis. J. Bacteriol. 126:758-770.
33. Parkinson, J. S., P. Ames, and C. A. Studdert. 2005. Collaborative signaling by bacterial chemoreceptors. Curr. Opin. Microbiol. 8:116-121.
34. Parkinson, J. S., and S. E. Houts. 1982. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J. Bacteriol. 151:106-113.
35. Rebbapragada, A., M. S. Johnson, G. P. Harding, A. J. Zuccarelli, H. M. Fletcher, I. B. Zhulin, and B. L. Taylor. 1997. 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 94:10541-10546.
36. Schwede, T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
37. Shrout, A. L., D. J. Montefusco, and R. M. Weis. 2003. Template-directed assembly of receptor signaling complexes. Biochemistry 42:13379-13385.
38. Studdert, C. A., and J. S. Parkinson. 2004. Crosslinking snapshots of bacterial chemoreceptor squads. Proc. Natl. Acad. Sci. USA 101:2117-2122.
39. Studdert, C. A., and J. S. Parkinson. 2005. Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc. Natl. Acad. Sci. USA 102:15623-15628.
40. Surette, M. G., and J. B. Stock. 1996. Role of alpha-helical coiled-coil interactions in receptor dimerization, signaling, and adaptation during bacterial chemotaxis. J. Biol. Chem. 271:17966-17973.
41. Swain, K. E., and J. J. Falke. 2007. Structure of the conserved HAMP domain in an intact, membrane-bound chemoreceptor: a disulfide mapping study. Biochemistry 46:13684-13695.
42. Umemura, T., Y. Matsumoto, K. Ohnishi, M. Homma, and I. Kawagishi. 2002. Sensing of cytoplasmic pH by bacterial chemoreceptors involves the linker region that connects the membrane-spanning and the signal-modulating helices. J. Biol. Chem. 277:1593-1598.
43. Utsumi, R., R. E. Brissette, A. Rampersaud, S. A. Forst, K. Oosawa, and M. Inouye. 1989. Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate. Science 245:1246-1249.
44. Ward, S. M., A. Delgado, R. P. Gunsalus, and M. D. Manson. 2002. A NarX-Tar chimera mediates repellent chemotaxis to nitrate and nitrite. Mol. Microbiol. 44:709-719.
45. Watts, K. J., M. S. Johnson, and B. L. Taylor. 2008. Structure-function relationships in the HAMP and proximal signaling domains of the aerotaxis receptor Aer. J. Bacteriol. 190:2118-2127.
46. Williams, S. B., and V. Stewart. 1999. 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. 33:1093-1102.
47. Wolanin, P. M., M. D. Baker, N. R. Francis, D. R. Thomas, D. J. DeRosier, and J. B. Stock. 2006. Self-assembly of receptor/signaling complexes in bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 103:14313-14318.
48. Yen, K. M. 1991. Construction of cloning cartridges for development of expression vectors in gram-negative bacteria. J. Bacteriol. 173:5328-5335.
49. Zhu, Y., and M. Inouye. 2003. Analysis of the role of the EnvZ linker region in signal transduction using a chimeric Tar/EnvZ receptor protein, Tez1. J. Biol. Chem. 278:22812-22819.