Ultrasensitivity in Phosphorylation-Dephosphorylation Cycles with Little Substrate

PLoS Computational Biology

Volumn 9, Issue 8, 2013, Pages

  Martins, Bruno M C ^a   Swain, Peter S ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DECISION MAKING; ENZYMES; NUMERICAL METHODS; PHOSPHORYLATION;

BUDDING YEASTS; CELL-FATE; CELLULARS; CIRCADIAN RHYTHMS; DECISIONS MAKINGS; DEPHOSPHORYLATIONS; DYNAMIC BEHAVIORS; IN-VIVO; ULTRASENSITIVE; ULTRASENSITIVITY;

SUBSTRATES;

PHOSPHATASE; PHOSPHOTRANSFERASE;

ALLOSTERISM; ANALYTIC METHOD; ARTICLE; BINDING AFFINITY; BIOINFORMATICS; CELL FATE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME REGULATION; ENZYME SUBSTRATE COMPLEX; EUKARYOTIC CELL; HILL REACTION; MATHEMATICAL ANALYSIS; MICHAELIS CONSTANT; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCETALES;

EID: 84883362218     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003175     Document Type: Article

References (45)

1. Bhalla US, Iyengar R, (1999) Emergent properties of networks of biological signaling pathways. Science 283: 381-387.
2. Groban ES, Narayanan A, Jacobson MP, (2006) Conformational changes in protein loops and helices induced by post-translational phosphorylation. PLoS Comput Biol 2: e32.
3. Goldbeter A, Koshland DE, (1981) An amplified sensitivity arising from covalent modification in biological systems. Proc Natl Acad Sci U S A 78: 6840-6844.
4. Ferrell JE, (2002) Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 14: 140-148.
5. Ferrell JE, (1997) How responses get more switch-like as you move down a protein kinase cascade. Trends Biochem Sci 22: 288-289.
6. Salazar C, Höfer T, (2009) Multisite protein phosphorylation-from molecular mechanisms to kinetic models. FEBS J 276: 3177-3198.
7. Lenz P, Swain PS, (2006) An entropic mechanism to generate highly cooperative and specific binding from protein phosphorylations. Curr Biol 16: 2150-2155.
8. Salazar C, Höfer T, (2006) Kinetic models of phosphorylation cycles: A systematic approach using the rapid-equilibrium approximation for protein-protein interactions. Biosystems 83: 195-206.
9. Blüthgen N, Bruggeman FJ, Legewie S, Herzel H, Westerhoff HV, et al. (2006) Effects of sequestration on signal transduction cascades. FEBS J 273: 895-906.
10. Liu X, Bardwell L, Nie Q, (2010) A combination of multisite phosphorylation and substrate sequestration produces switchlike responses. Biophys J 98: 1396-1407.
11. Berg JM, Tymoczko JL, Stryer L, Clarke ND (2002) Biochemistry. New York: W H Freeman. Section 8.4.
12. LaPorte DC, Koshland D Jr, (1983) Phosphorylation of isocitrate dehydrogenase as a demonstration of enhanced sensitivity in covalent regulation. Nature 305: 286-290.
13. Meinke MH, Bishop JS, Edstrom RD, (1986) Zero-order ultrasensitivity in the regulation of glycogen phosphorylase. Proc Natl Acad Sci U S A 83: 2865-2868.
14. Melen GJ, Levy S, Barkai N, Shilo BZ, (2005) Threshold responses to morphogen gradients by zero-order ultrasensitivity. Mol Syst Biol 1: 2005.0028.
15. Cimino A, Hervagault JF, (1987) Experimental evidence for a zero-order ultrasensitivity in a simple substrate cycle. Biochem Biophys Res Commun 149: 615-620.
16. Malleshaiah MK, Shahrezaei V, Swain PS, Michnick SW, (2010) The scaffold protein Ste5 directly controls a switch-like mating decision in yeast. Nature 465: 101-105.
17. Dushek O, van der Merwe PA, Shahrezaei V, (2011) Ultrasensitivity in multisite phosphorylation of membrane-anchored proteins. Biophys J 100: 1189-1197.
18. Stark C, Breitkreutz BJ, Chatr-Aryamontri A, Boucher L, Oughtred R, et al. (2011) The BioGRID interaction database: 2011 update. Nucleic Acids Res 39: D698-D704.
19. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
20. Monod J, Wyman J, Changeux JP, (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88-118.
21. Volkman BF, Lipson D, Wemmer DE, Kern D, (2001) Two-state allosteric behavior in a single-domain signaling protein. Science 291: 2429-2433.
22. Changeux JP, Edelstein SJ, (2005) Allosteric mechanisms of signal transduction. Science 308: 1424-1428.
23. Gunasekaran K, Ma B, Nussinov R, (2004) Is allostery an intrinsic property of all dynamic proteins? Proteins 57: 433-443.
24. Koshland DE Jr, Némethy G, Filmer D, (1966) Comparison of Experimental Binding Data and Theoretical Models in Proteins Containing Subunits. Biochemistry 5: 365-385.
25. Marzen S, Garcia HG, Phillips R, (2013) Statistical Mechanics of Monod-Wyman-Changeux (MWC) Models. J Mol Biol 425: 1433-1460.
26. Martins BM, Swain PS, (2011) Trade-offs and constraints in allosteric sensing. PLoS Comput Biol 7: e1002261.
27. Salazar C, Höfer T, (2003) Allosteric regulation of the transcription factor NFAT1 by multiple phosphorylation sites: a mathematical analysis. J Mol Biol 327: 31-45.
28. Remenyi A, Good MC, Lim WA, (2006) Docking interactions in protein kinase and phosphatase networks. Curr Opin Struct Biol 16: 676-685.
29. Ubersax JA, Ferrell JE Jr, (2007) Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8: 530-541.
30. Kim SY, Ferrell JE, (2007) Substrate competition as a source of ultrasensitivity in the inactivation of Wee1. Cell 128: 1133-1145.
31. Wang L, Nie Q, Enciso G, (2010) Nonessential sites improve phosphorylation switch. Biophys J 99: L41-L43.
32. Huang C-Y, Ferrell JE, (1996) Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc Natl Acad Sci U S A 93: 10078-10083.
33. Patwardhan P, Miller W, (2007) Processive phosphorylation: mechanism and biological importance. Cell Signal 19: 2218-2226.
34. Beard DA, Qian H (2008) Chemical biophysics: quantitative analysis of cellular systems. Cambridge: Cambridge University Press. pp. 84.
35. Szomolay B, Shahrezaei V, (2012) Bell-shaped and ultrasensitive dose-response in phosphorylation-dephosphorylation cycles: the role of kinase-phosphatase complex formation. BMC Syst Biol 6: 26.
36. Ferrell JE, Bhatt RR, (1997) Mechanistic studies of the dual phosphorylation of mitogen-activated protein kinase. J Biol Chem 272: 19008-19016.
37. Jeffery DA, Springer M, King DS, O'Shea EK, (2001) Multi-site phosphorylation of Pho4 by the cyclin-CDK Pho80-Pho85 is semi-processive with site preference. J Mol Biol 306: 997-1010.
38. Salazar C, Höfer T, (2007) Versatile regulation of multisite protein phosphorylation by the order of phosphate processing and protein-protein interactions. FEBS J 274: 1046-1061.
39. Tanoue T, Adachi M, Moriguchi T, Nishida E, (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat Cell Biol 2: 110-116.
40. Zalatan JG, Coyle SM, Rajan S, Sidhu SS, Lim WA, (2012) Conformational Control of the Ste5 Scaffold Protein Insulates Against MAP Kinase Misactivation. Science 337: 1218-1222.
41. Bhattacharyya RP, Reményi A, Good MC, Bashor CJ, Falick AM, et al. (2006) The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311: 822-826.
42. Chan C, Liu X, Wang L, Bardwell L, Nie Q, et al. (2012) Protein scaffolds can enhance the bistability of multisite phosphorylation systems. PLoS Comput Biol 8: e1002551.
43. Buchler NE, Cross FR, (2009) Protein sequestration generates a flexible ultrasensitive response in a genetic network. Mol Syst Biol 5: 272.
44. Gunawardena J, (2005) Multisite protein phosphorylation makes a good threshold but can be a poor switch. Proc Natl Acad Sci U S A 102: 14617-14622.
45. Siso-Nadal F, Ollivier JF, Swain PS, (2007) Facile: a command-line network compiler for systems biology. BMC Syst Biol 1: 36.