Large increases in attractant concentration disrupt the polar localization of bacterial chemoreceptors

Molecular Microbiology

Volumn 57, Issue 3, 2005, Pages 774-785

  Lamanna, Allison C ^a   Ordal, George W ^b   Kiessling, Laura L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; METHYL ACCEPTING CHEMOTAXIS PROTEIN; PARAFORMALDEHYDE; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL STRAIN; CHEMORECEPTOR; CHEMOTAXIS; CONTROLLED STUDY; CROSS LINKING; ESCHERICHIA COLI; MOLECULAR MODEL; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RECEPTOR OCCUPANCY; SIGNAL TRANSDUCTION;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL POLARITY; CHEMORECEPTORS; CHEMOTACTIC FACTORS; CHEMOTAXIS; ESCHERICHIA COLI; MEMBRANE PROTEINS; MUTATION; SIGNAL TRANSDUCTION;

BACILLUS SUBTILIS; ESCHERICHIA COLI;

EID: 22644447561     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04728.x     Document Type: Article

References (79)

1. Adler, J., Hazelbauer, G.L., and Dahl, M.M. (1973) Chemotaxis towards sugars in Escherichia coli. J Bacteriol 115: 824-847.
2. Alam, M., and Hazelbauer, G.L. (1991) Structural features of methyl-accepting taxis proteins conserved between Archaebacteria and Eubacteria revealed by antigenic cross-reaction. J Bacteriol 173: 5837-5842.
3. Albert, R., Chiu, Y.W., and Othmer, H.G. (2004) Dynamic receptor team formation can explain the high signal transduction gain in Escherichia coli. Biophys J 86: 2650-2659.
4. Ames, P., Studdert, C.A., Reiser, R.H., and Parkinson, U.S. (2002) Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99: 7060-7065.
5. Armitage, J.P., and Schmitt, R. (1997) Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti - variations on a theme? Microbiology 143: 3671-3682.
6. Barak, R., and Eisenbach, M. (1992) Correlation between phosphorylation of the chemotaxis protein CheY and its activity at the flagellar motor. Biochemistry 31: 1822-1826.
7. Biemann, H.P., and Koshland, D.E. (1994) Aspartate receptors of Escherichia coli and Salmonella typhimurium bind ligand with negative and half-of-the-sites cooperativity. Biochemistry 33: 629-634.
8. Bischoff, D.S., and Ordal, G.W. (1991) Sequence and characterization of Bacillus subtilis CheB, a homolog of Escherichia coli CheY, and its role in a difference mechanism of chemotaxis. J Biol Chem 266: 12301-12305.
9. Bischoff, D.S., and Ordal, G.W. (1992) Bacillus subtilis chemotaxis: a deviation from the Escherichia coli paradigm. Mol Microbiol 6: 23-28.
10. 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.
11. Bray, D. (2002) Bacterial chemotaxis and the question of gain. Proc Natl Acad Sci USA 99: 7-9.
12. Bray, D., Levin, M.D., and Morton-Firth, C.J. (1998) Receptor clustering as a cellular mechanism to control sensitivity. Nature 393: 85-88.
13. Bunn, M.W., and Ordal, G.W. (2003) Transmembrane organization of the Bacillus subtilis chemoreceptor McpB deduced by cysteine disulfide crosslinking. J Mol Biol 331: 941-949.
14. Bunn, M.W., and Ordal, G.W. (2004) Receptor conformation changes enhance methylesterase activity during chemotaxis by Bacillus subtilis. Mol Microbiol 51: 721-728.
15. Burgess-Gassier, A., Ullah, A.M., and Ordal, G.W. (1982) Purification and characterization of Bacillus subtilis methyl-accepting chemotaxis protein methyltransferase II. J Biol Chem 257: 8412-8417.
16. Cheng, P.C., Dykstra, M.L., Mitchell, R.N., and Pierce, S.K. (1999) A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J Exp Med 190: 1549-1560.
17. Duke, T.A.J., and Bray, D. (1999) Heightened sensitivity of a lattice of membrane receptors. Proc Natl Acad Sci USA 96: 10104-10108.
18. Edidin, M. (1997) Lipid microdomains in cell surface membranes. Curr Opin Struct Biol 7: 528-532.
19. Falke, J.J., and Koshland, D.E., Jr (1987) Global flexibility in a sensory receptor: a site-directed crosslinking approach. Science 237: 1596-1600.
20. Field, K.A., Holowka, D., and Baird, B. (1997) Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J Biol Chem 272: 4276-4280.
21. D-dependent gene encodes a novel protein with both CheW and CheY homologous domains. J Bacteriol 176: 2727-2735.
22. Fuhrer, D.K., and Ordal, G.W. (1991) Bacillus subtilis CheN, a homolog of CheA, the central regulator of chemotaxis in Escherichia coli. J Bacteriol 173: 7443-7448.
23. Garrity, L.F., and Ordal, G.W. (1997) Activation of the CheA kinase by asparagine in Bacillus subtilis chemotaxis. Microbiology 143: 2945-2951.
24. 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.
25. Gestwicki, J.E., and Kiessling, L.L. (2002) Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415: 81-84.
26. Gestwicki, J.E., Lamanna, A.C., Harshey, R.M., McCarter, L.L., Kiessling, L.L., and Adler, J. (2000) Evolutionary conservation of methyl-accepting chemotaxis protein location in Bacteria and Archaea. J Bacteriol 182: 6499-6502.
27. Giurisato, E., McIntosh, D.P., Tassi, M., Gamberucci, A., and Benedetti, A. (2003) T cell receptor can be recruited to a subset of plasma membrane rafts, independently of cell signaling and attendantly to raft clustering. J Biol Chem 278: 6771-6778.
28. Goldman, D.J., Worobec, S.W., Siegel, R.B., Hecker, R.V., and Ordal, G.W. (1982) Chemotaxis in Bacillus subtilis: effects of attractants on the level of methylation of methyl-accepting chemotaxis proteins and the role of demethylation in the adaptation process. Biochemistry 21: 915-920.
29. Hanlon, D.W., Márquez-Magaña, L.M., Carpenter, P.B., Chamberlin, M.J., and Ordal, G.W. (1992a) Sequence and characterization of Bacillus subtilis CheW. J Biol Chem 267: 12055-12060.
30. Hanlon, D.W., Carpenter, P.B., and Ordal, G.W. (1992b) Influence of attractants and repellents on methyl group turnover on methyl-accepting chemotaxis proteins of Bacillus subtilis and role of CheW. J Bacteriol 174: 4218-4222.
31. Harrison, D., Skidmore, J., Armitage, J., and Maddock, J. (1999) Localization and environmental regulation of MCP-like proteins in Rhodobacter sphaeroides. Mol Microbiol 31: 885-892.
32. Hazelbauer, G.L., and Engström, P. (1981) Multiple forms of methyl-accepting chemotaxis proteins distinguished by a factor in addition to multiple methylation. J Bacteriol 145: 35-42.
33. Homma, M., Shiomi, D., Homma, M., and Kawagishi, I. (2004) Attractant binding alters arrangement of chemoreceptor dimers within its cluster at a cell pole. Proc Natl Acad Sci USA 101: 3462-3467.
34. 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 USA 93: 11546-11551.
35. Jasuja, R., Lin, Y., Trentham, D.R., and Khan, S. (1999) Response tuning in bacterial chemotaxis. Proc Natl Acad Sci USA 96: 11346-11351.
36. Karatan, E., Saulmon, M.M., Bunn, M.W., and Ordal, G.W. (2001) Phosphorylation of the response regulator CheV is required for adaptation to attractants during Bacillus subtilis chemotaxis. J Biol Chem 276: 43618-43626.
37. 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.
38. Kim, C., Jackson, M., Lux, R., and Khan, S. (2001) Determinants of chemotactic signal amplification in Escherichia coli. J Mol Biol 307: 119-135.
39. 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 USA 99: 11611-11615.
40. Kirby, U.R., Niewold, T.B., Maloy, S., and Ordal, G.W. (2000) CheB is required for behavioral responses to negative stimuli during chemotaxis in Bacillus subtilis. Mol Microbiol 35: 44-57.
41. Lamanna, A.C., Gestwicki, J.E., Strong, L.E., Borchardt, S.L., Owen, R.M., and Kiessling, L.L. (2002) Conserved amplification of chemotactic responses through chemoreceptor interactions. J Bacteriol 184: 4981-4987.
42. Lee, G.F., Lebert, M.R., Lilly, A.A., and Hazelbauer, G.L. (1995) Transmembrane signaling characterized in bacterial chemoreceptors using sulfhydryl cross-linking in vivo. Proc Natl Acad Sci USA 92: 3391-3395.
43. Leong, A.S.-Y. (1994) Fixation and fixatives. In Laboratory Histopathology: A Complete Reference, Vol. 4. Woods, E.A., and Ellis, R.C. (eds). Edinburgh: Churchill Livingstone, pp. 1-26.
44. Levit, M.N., Grebe, T.W., and Stock, J.B. (2002) Organization of the receptor-kinase signaling array that regulates Escherichia coli chemotaxis. J Biol Chem 277: 36748-36754.
45. Li, M.S., and Hazelbauer, G.L. (2004) Cellular stoichiometry of the components of the chemotaxis signaling complex. J Bacteriol 186: 3687-3694.
46. Lybarger, S.R., and Maddock, J.R. (2000) Differences in the polar clustering of the high- and low-abundance chemoreceptors of Escherichia coli. Proc Natl Acad Sci USA 97: 8057-8062.
47. Maddock, J.R., and Shapiro, L. (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717-1723.
48. Mello, B.A., and Tu, Y. (2003) Quantitative modeling of sensitivity in bacterial chemotaxis: the role of coupling among different chemoreceptor species. Proc Natl Acad Sci USA 100: 8223-8228.
49. Mesibov, R., and Adler, J. (1972) Chemotaxis toward amino acids in Escherichia coli. J Bacteriol 112: 315-326.
50. Mesibov, R., Ordal, G.W., and Adler, J. (1973) The range of attractant concentrations for bacterial chemotaxis and the threshold and size over this range. J Gen Physiol 62: 203-223.
51. Milligan, D.L., and Koshland, D.E., Jr (1988) Site-directed crosslinking. Establishing the dimeric structure of the aspartate receptor of bacterial chemotaxis. J Biol Chem 263: 6268-6275.
52. Morgan, D.G., Baumgartner, J.W., and Hazelbauer, G.L. (1993) Proteins antigenically related to methyl-accepting chemotaxis proteins of Escherichia coli detected in a wide range of bacterial species. J Bacteriol 175: 133-140.
53. Moual, H.L., 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.
54. Ordal, G.W., Villani, D.P., and Gibson, K.J. (1977) Amino acid chemoreceptors of Bacillus subtilis. J Bacteriol 129: 156-165.
55. Ordal, G.W., Parker, H.M., and Kirby, J.R. (1985) Complementation and characterization of chemotaxis mutants of Bacillus subtilis. J Bacteriol 164: 802-810.
56. Parkinson, J.S. (1993) Signal transduction schemes of bacteria. Cell 73: 857-871.
57. Pittman, M.S., Goodwin, M., and Kelly, D.J. (2001) Chemotaxis in the human gastric pathogen Helicobacter pylori: different roles for CheW and the three CheV paralogues, and evidence for CheV2 phosphorylation. Microbiology 147: 2493-2504.
58. Reth, M. (2001) Oligomeric antigen receptors: a new view on signaling for the selection of lymphocytes. Trends Immunol 22: 356-360.
59. Reth, M., Wienands, J., and Schamel, W.W.A. (2000) An unsolved problem of the clonal selection theory and the model of an oligomeric B-cell antigen receptor. Immunol Rev 176: 10-18.
60. Rosario, M.M.L., Fredrick, K.L., Ordal, G.W., and Helmann, J.D. (1994) Chemotaxis in Bacillus subtilis requires either of two functionally redundant CheW homologs. J Bacteriol 176: 2736-2739.
61. Rosario, M.M.L., Kirby, J.R., Bochar, D.A., and Ordal, G.W. (1995) Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD. Biochemistry 34: 3823-3831.
62. 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 by surface plasmon resonance. Nature 365: 343-347.
63. Segall, J.E., Block, S.M., and Berg, H.C. (1986) Temporal comparisons in bacterial chemotaxis. Proc Natl Acad Sci USA 83: 8987-8991.
64. Shi, Y., and Duke, T. (1998) Cooperative model of bacterial sensing. Phys Rev E 58: 6399-6406.
65. Skidmore, J.M., Ellefson, D.D., McNamara, B.P., Couto, M.M.P., Wolfe, A.J., and Maddock, J.R. (2000) Polar clustering of the chemoreceptors complex in Escherichia coli occurs in the absence of complete CheA function. J Bacteriol 182: 967-973.
66. Slocum, M.K., and Parkinson, J.S. (1983) Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: organization of the tar region. J Bacteriol 155: 565-577.
67. Sourjik, V., and Berg, H.C. (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99: 123-127.
68. Sourjik, V., and Berg, H. (2004) Functional interactions between receptors in bacterial chemotaxis. Nature 428: 437-441.
69. Springer, W.R., and Koshland, D.E., Jr (1977) Identification of a protein methyltransferase as the CheR gene product in the bacterial sensing system. Proc Natl Acad Sci USA 74: 533-537.
70. Stock, A.M. (1999) A nonlinear stimulus-response relation in bacterial chemotaxis. Proc Natl Acad Sci USA 96: 10945-10947.
71. Stock, J.B., and Koshland, D.E., Jr (1978) A protein methylesterase involved in bacterial sensing. Proc Natl Acad Sci USA 75: 3659-3663.
72. Studdert, C.A., and Parkinson, J.S. (2004) Crosslinking snapshots of bacterial chemoreceptor squads. Proc Natl Acad Sci USA 101: 2117-2122.
73. Szurmant, H., Muff, T.J., and Ordal, G.W. (2004a) Bacillus subtilis CheC and FliY are members of a novel class of CheY-P-hydrolyzing proteins in the chemotactic signal transduction cascade. J Biol Chem 279: 21787-21792.
74. Szurmant, H., Bunn, M.W., Cho, S.H., and Ordal, G.W. (2004b) Ligand-induced conformational changes in the Bacillus subtilis chemoreceptor McpB determined by disulfide crosslinking in vivo. J Mol Biol 344: 919-928.
75. Thoelke, M.S., Kirby, J.R., and Ordal, G.W. (1989) Novel methyl transfer during chemotaxis in Bacillus subtilis. Biochemistry 28: 5585-5589.
76. West, A.H., and Stock, A.M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369-376.
77. Wylie, D., Stock, A., Wong, C.-Y., and Stock, J. (1988) Sensory transduction in bacterial chemotaxis involves pho-photransfer between Che proteins. Biochem Biophys Res Commun 151: 891-896.
78. Zimmer, M.A., Tiu, J., Collins, M.A., and Ordal, G.W. (2000) Selective methylation changes on the Bacillus subtilis chemotaxis receptor McpB promote adaptation. J Biol Chem 275: 24264-24272.
79. Zimmer, M.A., Szurmant, H., Saulmon, M.M., Collins, M.A., Bant, J.S., and Ordal, G.W. (2002) The role of heterologous receptors in McpB-mediated signaling in Bacillus subtilis chemotaxis. Mol Microbiol 45: 555-568.