Ligand depletion in vivo modulates the dynamic range and cooperativity of signal transduction

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Edelstein, Stuart J ^a   Stefan, Melanie I ^a   Le Novère, Nicolas ^a  

^a EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTATE CARBAMOYLTRANSFERASE; CALMODULIN; LIGAND; BACTERIAL PROTEIN; MEMBRANE PROTEIN; METHYL ACCEPTING CHEMOTAXIS PROTEINS; METHYL-ACCEPTING CHEMOTAXIS PROTEINS;

ARTICLE; CALCIUM BINDING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DEPLETION; DISSOCIATION CONSTANT; DOSE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; MOTOR ACTIVITY; NONHUMAN; SIGNAL TRANSDUCTION; TRANSDUCER; ESCHERICHIA COLI; METABOLISM; PHYSIOLOGY; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); MAMMALIA;

BACTERIAL PROTEINS; CALMODULIN; ESCHERICHIA COLI; LIGANDS; MEMBRANE PROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 77649086371     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008449     Document Type: Article

References (62)

1. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12: 88-118.
2. Bray D, Duke T (2004) Conformational spread: the propagation of allosteric states in large multiprotein complexes. Annu Rev Biophys Biomol Struct 33: 53-73.
3. Changeux JP, Edelstein SJ (2005) Allosteric mechanisms of signal transduction. Science 308: 1424-8.
4. Hill A (1910) The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol 40: 4-7.
5. Edelstein S (1975) Cooperative interactions of hemoglobin. Annu Rev Biochem 44: 209-232.
6. Ferdinand W (1966) The interpretation of non-hyperbolic rate curves for two-substrate enzymes. a possible mechanism for phosphofructokinase. Biochem J 98: 278-83.
7. Whitehead EP (1978) Co-operativity and the methods of plotting binding and steady-state kinetic data. Biochem J 171: 501-4.
8. Weiss JN (1997) The hill equation revisited: uses and misuses. Faseb J 11: 835-41.
9. Qian H (2008) Cooperativity and specificity in enzyme kinetics: a single-molecule time-based perspective. Biophys J 95: 10-7.
10. Kamata K, Mitsuya M, Nishimura T, Eiki J, Nagata Y (2004) Structural basis for allosteric regulation of the monomeric allosteric enzyme human glucokinase. Structure 12: 429-38.
11. Kim YB, Kalinowski SS, Marcinkeviciene J (2007) A pre-steady state analysis of ligand binding to human glucokinase: evidence for a preexisting equilibrium. Biochemistry 46: 1423-31.
12. Goldbeter A, Koshland JDE (1981) An amplified sensitivity arising from covalent modification in biological systems. Proc Natl Acad Sci U S A 78: 6840-4.
13. Kim SY, Ferrell JJE (2007) Substrate competition as a source of ultrasensitivity in the inactivation of Wee1. Cell 128: 1133-45.
14. Buchler NE, Louis M (2008) Molecular titration and ultrasensitivity in regulatory networks. J Mol Biol 384: 1106-19.
15. Bluthgen N, Bruggeman FJ, Legewie S, Herzel H, Westerhoff HV, et al. (2006) Effects of sequestration on signal transduction cascades. FEBS J 273: 895-906.
16. Koshland JDE (1996) The structural basis of negative cooperativity: receptors and enzymes. Curr Opin Struct Biol 6: 757-61.
17. Kister J, Poyart C, Edelstein S (1987) An expanded two-state allosteric model for interactions of human hemoglobin A with nonsaturating concentrations of 2,3-diphosphoglycerate. J Biol Chem 262: 12085-12091.
18. Rao CV, Glekas GD, Ordal GW (2008) The three adaptation systems of bacillus subtilis chemotaxis. Trends Microbiol 16: 480-7.
19. Hansen CH, Endres RG, Wingreen NS (2008) Chemotaxis in Escherichia coli: a molecular model for robust precise adaptation. PLoS Comput Biol 4: e1.
20. Goldstein A, Barrett RW (1987) Ligand dissociation constants from competition binding assays: errors associated with ligand depletion. Mol Pharmacol 31: 603-9.
21. Swillens S (1995) Interpretation of binding curves obtained with high receptor concentrations: practical aid for computer analysis. Mol Pharmacol 47: 1197-203.
22. Martinez K, Corringer P, Edelstein S, Changeux JP, Merola F (2000) Structural differences in the two agonist binding sites of the torpedo nicotinic acetylcholine receptor revealed by time-resolved fluorescence spectroscopy. Biochemistry 39: 6979-90.
23. Legewie S, Bluthgen N, Herzel H (2005) Quantitative analysis of ultrasensitive responses. FEBS J 272: 4071-9.
24. Kentner D, Sourjik V (2006) Spatial organization of the bacterial chemotaxis system. Curr Opin Microbiol 9: 619-24.
25. Belas R, Zhulin IB, Yang Z (2008) Bacterial signaling and motility: sure bets. J Bacteriol 190: 1849-56.
26. Xia Z, Storm DR (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6: 267-76.
27. Gsponer J, Christodoulou J, Cavalli A, Bui JM, Richter B, et al. (2008) A coupled equilibrium shift mechanism in calmodulin-mediated signal transduction. Structure 16: 736-46.
28. Schachman H (1988) Can a simple model account for the allosteric transition of aspartate transcarbamoylase? J Biol Chem 263: 18583-18586.
29. Lipscomb W (1994) Aspartate transcarbamylase from Escherichia coli: activity and regulation. Adv Enzymol Relat Areas Mol Biol 68: 67-151.
30. Cluzel P, Surette M, Leibler S (2000) An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287: 1652-5.
31. Sourjik V, Berg HC (2002) Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer. Proc Natl Acad Sci U S A 99: 12669-74.
32. Thomas DR, Morgan DG, DeRosier DJ (1999) Rotational symmetry of the C ring and a mechanism for the flagellar rotary motor. Proc Natl Acad Sci U S A 96: 10134-9.
33. McEvoy MM, Bren A, Eisenbach M, Dahlquist FW (1999) Identification of the binding interfaces on CheY for two of its targets, the phosphatase CheZ and the flagellar switch protein fliM. J Mol Biol 289: 1423-33.
34. Duke TA, Le Novère N, Bray D (2001) Conformational spread in a ring of proteins: a stochastic approach to allostery. J Mol Biol 308: 541-53.
35. Alon U, Camarena L, Surette MG, Aguera y Arcas B, Liu Y, et al. (1998) Response regulator output in bacterial chemotaxis. EMBO J 17: 4238-48.
36. Scharf BE, Fahrner KA, Turner L, Berg HC (1998) Control of direction of flagellar rotation in bacterial chemotaxis. Proc Natl Acad Sci U S A 95: 201-6.
37. Clapham DE (2007) Calcium signaling. Cell 131: 1047-58.
38. Stefan MI, Edelstein SJ, Le Novère N (2008) An allosteric model of calmodulin explains differential activation of PP2B and CaMKII. Proc Natl Acad Sci U S A 105: 10768-73.
39. Porumb T (1994) Determination of calcium-binding constants by flow dialysis. Anal Biochem 220: 227-37.
40. Kakiuchi S, Yasuda S, Yamazaki R, Teshima Y, Kanda K, et al. (1982) Quantitative determinations of calmodulin in the supernatant and particulate fractions of mammalian tissues. J Biochem 92: 1041-8.
41. Karlin A (1967) On the application of "a plausible model" of allosteric proteins to the receptor of acetylcholine. J Theor Biol 16: 306-320.
42. Gerhart J, Pardee A (1962) The enzymology of control by feedback inhibition. J Biol Chem 237: 891-896.
43. Rubin M, Changeux JP (1966) On the nature of allosteric transitions: Implications of non-exclusive ligand binding. J Mol Biol 21: 265-274.
44. Gerhart J, Schachman H (1968) Allosteric interactions in aspartate transcarbamylase. II. evidence for different conformational states of the protein in the presence and absence of specific ligands. Biochemistry 7: 538-552.
45. Changeux JP, Rubin M (1968) Allosteric interactions in aspartate transcarbamylase. III. interpretations of experimental data in terms of the model of monod, wyman, and changeux. Biochemistry 7: 553-561.
46. Weber K (1968) New structural model of E. coli aspartate transcarbamylase and the amino-acid sequence of the regulatory polypeptide chain. Nature 218: 1116-9.
47. Wiley D, Lipscomb W (1968) Crystallographic determination of symmetry of aspartate transcarbamylase. Nature 218: 1119-1121.
48. Kantrowitz ER, Lipscomb WN (1990) Escherichia coli aspartate transcarbamoylase: the molecular basis for a concerted allosteric transition. Trends Biochem Sci 15: 53-9.
49. Fetler L, Kantrowitz ER, Vachette P (2007) Direct observation in solution of a preexisting structural equilibrium for a mutant of the allosteric aspartate transcarbamoylase. Proc Natl Acad Sci U S A 104: 495-500.
50. Cheng D, Hoogenraad CC, Rush J, Ramm E, Schlager MA, et al. (2006) Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol Cell Proteomics 5: 1158-70.
51. Goto S, Matsukado Y, Mihara Y, Inoue N, Miyamoto E (1986) The distribution of calcineurin in rat brain by light and electron microscopic immunohistochemistry and enzyme-immunoassay. Brain Res 397: 161-72.
52. Stefan MI, Edelstein SJ, Le Novère N (2009) Computing phenomenologic Adair-Klotz constants from microscopic MWC parameters. BMC Syst Biol 3: 68.
53. Salvetti S, Ghelardi E, Celandroni F, Ceragioli M, Giannessi F, et al. (2007) FlhF, a signal recognition particle-like GTPase, is involved in the regulation of flagellar arrangement, motility behaviour and protein secretion in Bacillus cereus. Microbiology 153: 2541-52.
54. Endres RG, Oleksiuk O, Hansen CH, Meir Y, Sourjik V, et al. (2008) Variable sizes of Escherichia coli chemoreceptor signaling teams. Mol Syst Biol 4: 211.
55. Markram H (2006) The blue brain project. Nat Rev Neurosci 7: 153-60.
56. Le Novere N (2007) The long journey to a systems biology of neuronal function. BMC Syst Biol 1: 28.
57. Izhikevich EM, Edelman GM (2008) Large-scale model of mammalian thalamocortical systems. Proc Natl Acad Sci U S A 105: 3593-8.
58. Giegling I, Hartmann AM, Genius J, Benninghoff J, Moller HJ, et al. (2008) Systems biology and complex neurobehavioral traits. Pharmacopsychiatry 41 Suppl 1: S32-6.
59. Villoslada P, Steinman L, Baranzini SE (2009) Systems biology and its application to the understanding of neurological diseases. Ann Neurol 65: 124-39.
60. Gamble E, Koch C (1987) The dynamics of free calcium in dendritic spines in response to repetitive synaptic input. Science 236: 1311-5.
61. Henkin RI (1997) The concentration of calmodulin present in parotid cells. J Dent Res 76: 1430.
62. Gerhart JC, Holoubek H (1967) The purification of aspartate transcarbamylase of Escherichia coli and separation of its protein subunits. J Biol Chem 242: 2886-92.