An allosteric model for transmembrane signaling in bacterial chemotaxis

Journal of Molecular Biology

Volumn 343, Issue 2, 2004, Pages 291-303

  Rao, Christopher V ^a,b   Frenklach, Michael ^b,c   Arkin, Adam P ^a,b,d  

^a University of California at Berkeley   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

allostery; chemotaxis; Monte Carlo; receptor clustering; signal transduction

Indexed keywords

CHEA KINASE; CHEW PROTEIN;

ALLOSTERISM; ARTICLE; BACTERIUM; CHEMOTAXIS; DIMERIZATION; METHYLATION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS);

EID: 4644278216     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.08.046     Document Type: Article

References (47)

1. A. Bren, and M. Eisenbach How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation J. Bacteriol. 182 2000 6865 6873
2. J.A. Gegner, D.R. Graham, A.F. Roth, and F.W. Dahlquist Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway Cell 70 1992 975 982
3. K.A. Borkovich, N. Kaplan, J.F. Hess, and M.I. Simon Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer Proc. Natl Acad. Sci. USA 86 1989 1208 1212
4. P. Cluzel, M. Surette, and S. Leibler An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells Science 287 2000 1652 1655
5. K.A. Borkovich, L.A. Alex, and M.I. Simon Attenuation of sensory receptor signaling by covalent modification Proc. Natl Acad. Sci. USA 89 1992 6756 6760
6. M.F. Goy, M.S. Springer, and J. Adler Sensory transduction in Escherichia coli: role of a protein methylation reaction in sensory adaptation Proc. Natl Acad. Sci. USA 74 1977 4964 4968
7. N. Barkai, U. Alon, and S. Leibler Robust amplification in adaptive signal transduction networks C. R. Acad. Sci. Paris, ser. IV 2 2001 817 877
8. N. Barkai, and S. Leibler Robustness in simple biochemical networks Nature 387 1997 913 917
9. D.C. Hauri, and J. Ross A model of excitation and adaptation in bacterial chemotaxis Biophys. J. 68 1995 708 722
10. C.J. Morton-Firth, T.S. Shimizu, and D. Bray A free-energy-based stochastic simulation of the Tar receptor complex J. Mol. Biol. 286 1999 1059 1074
11. T.S. Shimizu, S.V. Aksenov, and D. Bray A spatially extended stochastic model of the bacterial chemotaxis signalling pathway J. Mol. Biol. 329 2003 291 309
12. P.A. Spiro, J.S. Parkinson, and H.G. Othmer A model of excitation and adaptation in bacterial chemotaxis Proc. Natl Acad. Sci. USA 94 1997 7263 7268
13. R. Mesibov, G.W. Ordal, and J. Adler The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range. Weber law and related phenomena J. Gen. Physiol. 62 1973 203 223
14. J.E. Segall, S.M. Block, and H.C. Berg Temporal comparisons in bacterial chemotaxis Proc. Natl Acad. Sci. USA 83 1986 8987 8991
15. V. Sourjik, and H.C. Berg Receptor sensitivity in bacterial chemotaxis Proc. Natl Acad. Sci. USA 99 2002 123 127
16. J.A. Bornhorst, and J.J. Falke Attractant regulation of the aspartate receptor-kinase complex: limited cooperative interactions between receptors and effects of the receptor modification state Biochemistry 39 2000 9486 9493
17. M.R. Alley, J.R. Maddock, and L. Shapiro Polar localization of a bacterial chemoreceptor Genes Dev. 6 1992 825 836
18. J.R. Maddock, and L. Shapiro Polar location of the chemoreceptor complex in the Escherichia coli cell Science 259 1993 1717 1723
19. V. Sourjik, and H.C. Berg Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions Mol. Microbiol. 37 2000 740 751
20. D. Bray, M.D. Levin, and C.J. Morton-Firth Receptor clustering as a cellular mechanism to control sensitivity Nature 393 1998 85 88
21. T.A. Duke, and D. Bray Heightened sensitivity of a lattice of membrane receptors Proc. Natl Acad. Sci. USA 96 1999 10104 10108
22. S.H. Kim, W. Wang, and K.K. Kim Dynamic and clustering model of bacterial chemotaxis receptors: structural basis for signaling and high sensitivity Proc. Natl Acad. Sci. USA 99 2002 11611 11615
23. T.S. Shimizu, N. Le Novere, M.D. Levin, A.J. Beavil, B.J. Sutton, and D. Bray Molecular model of a lattice of signalling proteins involved in bacterial chemotaxis Nature Cell Biol. 2 2000 792 796
24. J.J. Falke Cooperativity between bacterial chemotaxis receptors Proc. Natl Acad. Sci. USA 99 2002 6530 6532
25. K.K. Kim, H. Yokota, and S.H. Kim Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor Nature 400 1999 787 792
26. P. Ames, C.A. Studdert, R.H. Reiser, and J.S. Parkinson Collaborative signaling by mixed chemoreceptor teams in Escherichia coli Proc. Natl Acad. Sci. USA 99 2002 7060 7065
27. C.A. Studdert, and J.S. Parkinson Crosslinking snapshots of bacterial chemoreceptor squads Proc. Natl Acad. Sci. USA 101 2004 2117 2122
28. P. Dunten, and D.E. Koshland Jr Tuning the responsiveness of a sensory receptor via covalent modification J. Biol. Chem. 266 1991 1491 1496
29. B.A. Mello, and Y. Tu Quantitative modeling of sensitivity in bacterial chemotaxis: the role of coupling among different chemoreceptor species Proc. Natl Acad. Sci. USA 100 2003 8223 8228
30. J.E. Gestwicki, and L.L. Kiessling Inter-receptor communication through arrays of bacterial chemoreceptors Nature 415 2002 81 84
31. V. Sourjik, and H.C. Berg Functional interactions between receptors in bacterial chemotaxis Nature 428 2004 437 441
32. R. Albert, Y. Chiu, and H.G. Othmer Dynamic receptor team formation can explain the high signal transduction gain in E. coli Biophys. J. 86 2004 2650 2659
33. Zhang, C. & Kim, S. H. (2000). The effect of dynamic receptor clustering on the sensitivity of biochemical signaling. Pac. Symp. Biocomput. 353-364.
34. J. Monod, J. Wyman, and J.P. Changeux On the nature of allosteric transitions: a plausible model J. Mol. Biol. 12 1965 88 118
35. J.J. Falke, and G.L. Hazelbauer Transmembrane signaling in bacterial chemoreceptors Trends Biochem. Sci. 26 2001 257 265
36. M. Homma, D. Shiomi, and I. Kawagishi Attractant binding alters arrangement of chemoreceptor dimers within its cluster at a cell pole Proc. Natl Acad. Sci. USA 101 2004 3462 3467
37. J.A. Bornhorst, and J.J. Falke Evidence that both ligand binding and covalent adaptation drive a two-state equilibrium in the aspartate receptor signaling complex J. Gen. Physiol. 118 2001 693 710
38. M.N. Levit, and J.B. Stock Receptor methylation controls the magnitude of stimulus-response coupling in bacterial chemotaxis J. Biol. Chem. 277 2002 36760 36765
39. H.P. Biemann, and D.E. Koshland Jr Aspartate receptors of Escherichia coli and Salmonella typhimurium bind ligand with negative and half-of-the-sites cooperativity Biochemistry 33 1994 629 634
40. Goldman, J., Andrews, S. & Bray, D. (2004). Size and composition of membrane protein clusters predicted by Monte Carlo analysis. Eur. Biophys. J. In the press.
41. G. Li, and R.M. Weis Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli Cell 100 2000 357 365
42. J.P. Armitage Bacterial Tactic Response Advances in Microbial Physiology vol. 41 1999 Academic Press London 229 289
43. M.A. Zimmer, H. Szurmant, M.M. Saulmon, M.A. Collins, J.S. Bant, and G.W. Ordal The role of heterologous receptors in McpB-mediated signalling in Bacillus subtilis chemotaxis Mol. Microbiol. 45 2002 555 568
44. C.V. Rao, J.R. Kirby, and A.P. Arkin Design and diversity in bacterial chemotaxis: a comparative study in Escherichia coli and Bacillus subtilis PLoS Biol. 2 2004 E49
45. B.N. Kholodenko Four-dimensional organization of protein kinase signaling cascades: the roles of diffusion, endocytosis and molecular motors J. Expt. Biol. 206 2003 2073 2082
46. M.D. Levin, T.S. Shimizu, and D. Bray Binding and diffusion of CheR molecules within a cluster of membrane receptors Biophys. J. 82 2002 1809 1817
47. D. Bray Bacterial chemotaxis and the question of gain Proc. Natl Acad. Sci. USA 99 2002 7 9