Intragenic suppressors of a mutation in the aspartate chemoreceptor gene that abolishes binding of the receptor to methyltransferase

Microbiology

Volumn 148, Issue 10, 2002, Pages 3265-3275

  Shiomi, Daisuke ^a   Homma, Michio ^a   Kawagishi, Ikuro ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Adaptation; Chemotaxis; Histidine kinase; Methylation; Revertant

Indexed keywords

ASPARAGINE; ASPARTIC ACID; GLUTAMIC ACID; METHYLTRANSFERASE; PHENYLALANINE; PROTEIN HISTIDINE KINASE; THREONINE; TRYPTOPHAN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMORECEPTOR; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ESCHERICHIA COLI; GENE MUTATION; GENE REPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN MOTIF; RECEPTOR BINDING; SIGNAL TRANSDUCTION; STOP CODON;

ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

EID: 0036773079     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-148-10-3265     Document Type: Article

References (60)

1. Alon, U., Surette, M. G., Barkai, N. & Leibler, S. (1999). Robustness in bacterial chemotaxis. Nature 397, 168-171.
2. Anand, G. S., Goudreau, P. N. & Stock, A. M. (1998). Activation of methyltransferase CheB: evidence of a dual role for the regulatory domain. Biochemistry 37, 14038-14047.
3. Barak, R. & Eisenbach, M. (1992). Correlation between phosphorylation of the chemotaxis protein CheY and its activity at the flagellar motor. Biochemistry 31, 1821-1826.
4. Barkai, N. & Leibler, S. (1997). Robustness in simple biochemical networks. Nature 387, 913-917.
5. Barnakov, A. N., Barnakova, L. A. & Hazelbauer, G. L. (1999). Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proc Natl Acad Sci U S A 96, 10667-10672.
6. Barnakov, A. N., Barnakova, L. A. & Hazelbauer, G. L. (2001). Location of the receptor-interaction site on CheB, the methylesterase response regulator of bacterial chemotaxis. J Biol Chem 276, 32984-32989.
7. Bass, R. B. & 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.
8. Bass, R. B. & Falke, J. J. (1999). The aspartate receptor cytoplasmic domain: in situ chemical analysis of structure, mechanism and dynamics. Structure 7, 829-840.
9. Blair, D. F. (1995). How bacteria sense and swim. Annu Rev Microbiol 49, 489-522.
10. Borkovich, K. A., Kaplan, N., Hess, J. F. & 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.
11. Borkovich, K. A., Alex, L. A. & Simon, M. I. (1992). Attenuation of sensory receptor signaling by covalent modification. Proc Natl Acad Sci U S A 89, 6756-6760.
12. Boyd, A. & Simon, M. I. (1980). Multiple electrophoretic forms of methyl-accepting chemotaxis proteins generated by stimulus-elicited methylation in Escherichia coli. J Bacteriol 143, 809-815.
13. Bulter, S. L. & Falke, J. J. (1998). Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor. Biochemistry 37, 10746-10756.
14. Chelsky, D. & Dahlquist, F. W. (1980). Structural studies of methyl-accepting chemotaxis proteins of Escherichia coli evidence for multiple methylation sites. Proc Natl Acad Sci U S A 77, 2434 2438.
15. Danielson, M. A., Bass, R. B. & 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.
16. DeFranco, A. L. & Koshland, D. E., Jr (1980). Multiple methylation in processing of sensory signals during bacterial chemotaxis. Proc Natl Acad Sci U S A 77, 2429-2433.
17. Djordjevic, S. & Stock, A. M. (1998). Chemotaxis receptor recognition by protein methyltransferase CheR. Nature Struct Biol 5, 446-450.
18. Engström, P. & Hazelbauer, G. L. (1980). Multiple methylation of methyl-accepting chemotaxis proteins during adaptation of E. coli to chemical stimuli. Cell 20, 165-171.
19. Falke, J. J., Bass, R. B., Butler, S. L., Chervitz, S. A. & 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.
20. Feng, X., Baumgartner, J. W. & Hazelbauer, G. L. (1997). High-and low-abundance chemoreceptors in Escherichia coli: differential activities associated with closely related cytoplasmic domains. J Bacteriol 179, 6714-6720.
21. Feng, X., Lilly, A. A. & Hazelbauer, G. L. (1999). Enhanced function conferred on low abundance chemoreceptor Trg by a methyl-transferase-docking site. J Bacteriol 181, 3164-3171.
22. Gegner, J. A., Graham, D. R., Roth, A. F. & Dahlquist, F. W. (1992). Assembly of an MCP, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell 70, 975-982.
23. Hazelbauer, G. L. & Engström, P. (1980). Parallel pathways for transduction of chemotactic signals in Escherichia coli. Nature 283, 98-100.
24. Hess, J. F., Oosawa, K., Kaplan, N. & Simon, M. I. (1988). Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53, 79-87.
25. Iwama, T., Homma, M. & Kawagishi, I. (1997). Uncoupling of ligand-binding affinity of the bacterial serine chemoreceptor from methylation- and temperature-modulated signaling states. J Biol Chem 272, 13810-13815.
26. Kim, K. K., Yokota, H. & Kim, S.-H. (1999). Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400, 787-792.
27. Kondoh, H., Ball, C. B. & Adler, J. (1979). Identification of a methyl-accepting chemotaxis protein for the ribose and galactose chemoreceptors of Escherichia coli. Proc Natl Acad Sci U S A 76, 260-264.
28. Landt, O., Grunert, H. P. & Hahn, U. (1990). A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene 96, 125-128.
29. Le Moual, H. & Koshland, D. E., Jr (1997). Methylation of the Escherichia coli chemotaxis receptors: intra- and interdimer mechanisms. Biochemistry 36, 13441-13448.
30. Li, J., Li, G. & Weis, R. M. (1997). The serine receptor from Escherichia coli is methylated through an inter-dimer process. Biochemistry 36, 11851-11857.
31. Liu, Y., Levit, M., Lurz, R., Surette, M. G. & Stock, J. B. (1997). Receptor-mediated protein kinase activation and the mechanism of transmembrane signaling in bacterial chemotaxis. EMBO J 16, 7231-7240.
32. Lupas, A. & Stock, J. (1989). Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. J Biol Chem 264, 17337-17342.
33. Lybarger, S. R. & Maddock, J. R. (2000). Differences in the polar clustering of the high- and low-abundance chemoreceptors of Escherichia coli. Proc Natl Acad Sci U S A 97, 8057-8062.
34. Maddock, J. R. & Shapiro, L. (1993). Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259, 1717-1723.
35. Manson, M. D. (1992). Bacterial motility and chemotaxis. Adv Microb Physiol 33, 277-346.
36. Milligan, D. L. & Koshland, D. E., Jr (1988). Site-directed cross linking: establishing the dimeric structure of the aspartate receptor of bacterial chemotaxis. J Biol Chem 263, 6268-6275.
37. Nishiyama, S., Nara, T., Imae, Y., Homma, M. & Kawagishi, I. (1997). Thermosensing properties of mutant aspartate receptors having methyl-accepting; sites substituted multiply or singly with alanine. J Bacteriol 179, 6573-6580.
38. Nishiyama, S., Umemura, T., Nara, T., Homma, M. & 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. Okumura, H., Nishiyama, S., Sasaki, A., Homma, M. & Kawagishi, I. (1998). Chemotactic adaptation is altered by changes in the C-terminal sequence conserved among the major methyl accepting chemoreceptors. J Bacteriol 180, 1862-1868.
40. Oosawa, K. & Simon, M. I. (1986). Analysis of mutations in the transmembrane region of aspartate chemoreceptor in Escherichia coli. Proc Natl Acad Sci U S A 83, 6930-6934.
41. Parkinson, J. S. (1993). Signal transduction schemes of bacteria. Cell 73, 857-871.
42. Schuster, S. C., Swanson, R. V., Alex, L. A., Bourret, R. B. & Simon, M. I. (1993). Assembly and function of a quaternary signal transduction complex monitored by surface plasmon resonance. Nature 365, 343-347.
43. Shiomi, D., Okumura, H., Homma, M. & Kawagishi, I. (2000). The aspartate chemoreceptor Tar is effectively methylated by binding to the methyltransferase mainly through hydrophobic interaction. Mol Microbiol 36, 132-140.
44. Shiomi, D., Zhulin, I. B., Homma, M. & Kawagishi, I. (2002). Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J Biol Chem (in press).
45. Simms, S. A., Stock, A. M. & Stock, J. B. (1987). Purification and characterization of S-adenosylmethionine:glutamyl methyltransferase that modifies membrane chemoreceptor proteins in bacteria. J Biol Chem 262, 8537-8543.
46. Springer, M. S., Goy, M. F. & Adler, J. (1977). Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc Natl Acad Sci U S A 74, 3312-3316.
47. Springer, W. R. & Koshland, D. E., Jr (1977). Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc Natl Acad Sci U S A 74, 533-537.
48. Stock, A. M., Wylie, D. C., Mottonen, J. M., Lupas, A. M., Ninfa, E. G., Ninfa, A. J., Schutt, C. E. & Stock, J. B. (1988). Phosphoproteins involved in bacterial signal transduction. Cold Spring Harbor Symp Quant Biol 53, 49-57.
49. Stock, J. B. & Surette, M. G. (1996). Chemotaxis. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd edn, pp. 1103-1129. Edited by F. C. Neidhardt & others. Washington, DC: American Society for Microbiology.
50. Tatsuno, I., Homma, M., Oosawa, K. & Kawagishi, I. (1996). Signaling by the Escherichia coli aspartate chemoreceptor Tar with a single cytoplasmic domain per dimer. Science 274, 423-425.
51. Trammell, M. A. & Falke, J. J. (1999). Identification of a site critical for kinase regulation on the central processing unit (CPU) helix of the aspartate receptor. Biochemistry 38, 329-336.
52. Umemura, T., Tatsuno, I., Shibasaki, M., Homma, M. & Kawagishi, I. (1998). Intersubunit interaction between transmembrane helices of the bacterial aspartate chemoreceptor homodimer. J Biol Chem 273, 30110-30115.
53. Wang, E. A. & Koshland, D. E., Jr (1980). Receptor structure in the bacterial sensing system. Proc Natl Acad Sci U S A 77, 7157-7161.
54. Weerasuriya, S., Schneider, B. M. & Manson, M. D. (1998). Chimeric chemoreceptors in Escherichia coli: signaling and methylation properties of Tar-Tap and Tap-Tar hybrids. J Bacteriol 180, 914-920.
55. Welch, M., Oosawa, K., Aizawa, S.-I. & Eisenbach, M. (1993). Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci U S A 90, 8787-8791.
56. Wolfe, A. J. & Berg, H. C. (1989). Migration of bacteria in semisolid agar. Proc Natl Acad Sci U S A 86, 6973-6977.
57. Wolfe, A. J., Conley, M. P., Kramer, T. J. & Berg, H. C. (1987). Reconstitution of signaling in bacterial chemotaxis. J Bacteriol 169, 1878-1885.
58. Wu, J., Li, J., Li, G., Long, D. G. & Weis, R. M. (1996). The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 35, 4984-4993.
59. Wylie, D., Stock, A. M., Wong, C.-Y. & Stock, J. (1988). Sensory transduction in bacterial chemotaxis involves phosphotransfer between Che proteins. Biochem Biophys Res Commun 151, 891-896.
60. Yamamoto, K., Macnab, R. M. & Imae, Y. (1990). Repellent response functions of the Trg and Tap chemoreceptors of Escherichia coli. J Bacteriol 172, 383-388.