A dynamic-signaling-team model for chemotaxis receptors in Escherichia coli

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 40, 2010, Pages 17170-17175

  Hansen, Clinton H ^a   Sourjik, Victor ^b   Wingreen, Ned S ^c  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

Adaptation; Modeling; Receptor clustering

Indexed keywords

CHEMOATTRACTANT; DIMER; RECEPTOR;

ADAPTATION; ARTICLE; CHEMORECEPTOR; CHEMOTAXIS; CRYOELECTRON MICROSCOPY; DEMETHYLATION; ESCHERICHIA COLI; METHYLATION; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR OCCUPANCY; SIGNAL TRANSDUCTION; TOMOGRAPHY;

ALGORITHMS; CHEMOTACTIC FACTORS; CHEMOTAXIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, BIOLOGICAL; PROTEIN CONFORMATION; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI;

EID: 78049312249     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1005017107     Document Type: Article

References (39)

1. Smirnakis SM, Berry MJ, Warland DK, Bialek W, Meister M (1997) Adaptation of retinal processing to image contrast and spatial scale. Nature 386:69-73.
2. Kurahashi T, Menini A (1997) Mechanism of odorant adaptation in the olfactory receptor cell. Nature 385:725-729.
3. Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24:10440-10453.
4. Barkai N, Leibler S (1997) Robustness in simple biochemical networks. Nature 387:913-917.
5. Yi T-M, Huang Y, Simon MI, Doyle J (2000) Robust perfect adaptation in bacterial chemotaxis through integral feedback control. Proc Natl Acad Sci USA 97:4649-4653.
6. Sourjik V, Berg HC (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99:123-127.
7. Sourjik V, Berg HC (2004) Functional interactions between receptors in bacterial chemotaxis. Nature 428:437-441.
8. Sanders DA, Koshland DE (1988) Receptor interactions through phosphorylation and methylation pathways in bacterial chemotaxis. Proc Natl Acad Sci USA 85:8425-8429.
9. Studdert CA, Parkinson JS (2005) Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc Natl Acad Sci USA 102:15623-15628.
10. Boldog T, Grimme S, Li M, Sligar SG, Hazelbauer GL (2006) Nanodiscs separate chemoreceptor oligomeric states and reveal their signaling properties. Proc Natl Acad Sci USA 103:11509-11514.
11. Djordjevic S, Goudreau PN, Xu Q, Stock AM, West AH (1998) Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. Proc Natl Acad Sci USA 95:1381-1386.
12. Barnakov AN, Barnakova LA, Hazelbauer GL (1999) Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proc Natl Acad Sci USA 96:10667-10672.
13. Li M, Hazelbauer GL (2005) Adaptational assistance in clusters of bacterial chemoreceptors. Mol Microbiol 56:1617-1626.
14. Li G, Weis RM (2000) Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100:357-365.
15. Endres RG, et al. (2008) Variable sizes of Escherichia coli chemoreceptor signaling teams. Mol Syst Biol 4:211.
16. Shiomi D, Banno S, Homma M, Kawagishi I (2005) Stabilization of polar localization of a chemoreceptor via its covalent modifications and its communication with a different chemoreceptor. J Bacteriol 187:7647-7654.
17. Kentner D, Thiem S, Hildenbeutel M, Sourjik V (2006) Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 61:407-417.
18. Greenfield D, et al. (2009) Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol 7:e1000137.
19. Khursigara CM, Wu X, Subramaniam S (2008) Chemoreceptors in Caulobacter crescentus: trimers of receptor dimers in a partially ordered hexagonally packed array. J Bacteriol 190:6805-6810.
20. Briegel A, et al. (2008) Location and architecture of the Caulobacter crescentus chemoreceptor array. Mol Microbiol 69:30-41.
21. Briegel A, et al. (2009) Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 106:17181-17186.
22. Schulmeister S, et al. (2008) Protein exchange dynamics at chemoreceptor clusters in Escherichia coli. Proc Natl Acad Sci USA 105:6403-6408.
23. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88-118.
24. Mello BA, Tu Y (2005) An allosteric model for heterogeneous receptor complexes: understanding bacterial chemotaxis responses to multiple stimuli. Proc Natl Acad Sci USA 102:17354-17359.
25. Keymer JE, Endres RG, Skoge M, Meir Y, Wingreen NS (2006) Chemosensing in Escherichia coli: two regimes of two-state receptors. Proc Natl Acad Sci USA 103:1786-1791.
26. Endres RG, Wingreen NS (2006) Precise adaptation in bacterial chemotaxis through "assistance neighborhoods". Proc Natl Acad Sci USA 103:13040-13044.
27. Skoge ML, Endres RG, Wingreen NS (2006) Receptor-receptor coupling in bacterial chemotaxis: evidence for strongly coupled clusters. Biophys J 90:4317-4326.
28. Hansen CH, Endres RG, Wingreen NS (2008) Chemotaxis in Escherichia coli: a molecular model for robust precise adaptation. PLoS Comput Biol 4:e1.
29. Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E (1953) Equations of state calculations by fast computing machines. J Chem Phys 21:1087-1092.
30. Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81:2340-2361.
31. Dunten P, Koshland DE (1991) Tuning the responsiveness of a sensory receptor via covalent modification. J Biol Chem 266:1491-1496.
32. Endres RG (2009) Polar chemoreceptor clustering by coupled trimers of dimers. Biophys J 96:453-463.
33. Weis RM, et al. (2003) Electron microscopic analysis of membrane assemblies formed by the bacterial chemotaxis receptor Tsr. J Bacteriol 185:3636-3643.
34. Ursell T, Huang KC, Peterson E, Phillips R (2007) Cooperative gating and spatial organization of membrane proteins through elastic interactions. PLoS Comput Biol 3:e81.
35. Draheim RR, Bormans AF, Lai RZ, Manson MD (2006) Tuning a bacterial chemoreceptor with protein-membrane interactions. Biochemistry 45:14655-14664.
36. Vaknin A, Berg HC (2006) Osmotic stress mechanically perturbs chemoreceptors in Escherichia coli. Proc Natl Acad Sci USA 103:592-596.
37. Besschetnova TY, et al. (2008) Receptor density balances signal stimulation and attenuation in membrane-assembled complexes of bacterial chemotaxis signaling proteins. Proc Natl Acad Sci USA 105:12289-12294.
38. Shimizu TS, Aksenov SV, Bray D (2003) A spatially extended stochastic model of the bacterial chemotaxis signalling pathway. J Mol Biol 329:291-309.
39. Mello BA, Shaw L, Tu Y (2004) Effects of receptor interaction in bacterial chemotaxis. Biophys J 87:1578-1595.