Ultrasensitivity in multisite phosphorylation of membrane-anchored proteins

Biophysical Journal

Volumn 100, Issue 5, 2011, Pages 1189-1197

  Dushek, Omer ^a,b   Van Der Merwe, P Anton ^a   Shahrezaei, Vahid ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79953897645     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.01.060     Document Type: Article

References (46)

1. Melen, G. J., S. Levy, B.-Z. Shilo. 2005. Threshold responses to morphogen gradients by zero-order ultrasensitivity. Mol. Syst. Biol. 1:2005.0028.
2. Altan-Bonnet, G., and R. N. Germain. 2005. Modeling T cell antigen discrimination based on feedback control of digital ERK responses. PLoSBiol. 3:e356.
3. Tian, T., A. Harding, ..., J. F. Hancock. 2007. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat. Cell Biol. 9:905-914. (Pubitemid 47190445)
4. Kim, S. Y., and J. E. Ferrell, Jr. 2007. Substrate competition as a source of ultrasensitivity in the inactivation of Weel. Cell. 128:1133-1145. (Pubitemid 46437260)
5. Holt, L. J., A. N. Krutchinsky, and D. O. Morgan. 2008. Positive feedback sharpens the anaphase switch. Nature. 454:353-357.
6. Das, J., M. Ho, ..., J. P. Roose. 2009. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell. 136:337-351.
7. Malleshaiah, M. K., V. Shahrezaei, ..., S. W. Michnick. 2010. The scaffold protein Ste5 directly controls a switch-like mating decision in yeast. Nature. 465:101-105.
8. Weiss, A., and D. R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell. 76:263-274. (Pubitemid 24046689)
9. Veillette, A. 2006. Immune regulation by SLAM family receptors and SAP-related adaptors. Nat. Rev. Immunol. 6:56-66. (Pubitemid 43279753)
10. Davis, S. J., and P. A. van der Merwe. 2006. The kinetic-segregation model: TCR triggering and beyond. Nat. Immunol. 7:803-809. (Pubitemid 44084086)
11. Lemmon, M. A., and J. Schlessinger. 2010. Cell signaling by receptor tyrosine kinases. Cell. 141:1117-1134.
12. Guy, C. S., and D. A. A. Vignali. 2009. Organization of proximal signal initiation at the TCR:CD3 complex. Immunol. Rev. 232:7-21.
13. Feinerman, O., R. N. Germain, and G. Altan-Bonnet. 2008. Quantitative challenges in understanding ligand discrimination by αβ T cells. Mol. Immunol. 45:619-631. (Pubitemid 47498584)
14. van der Merwe, P. A., and O. Dushek. 2011. Mechanisms for T cell receptor triggering. Nat. Rev. Immunol. 11:47-55.
15. Goldbeter, A., and D. E. Koshland, Jr. 1981. An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. USA. 78:6840-6844. (Pubitemid 12216857)
16. Lauffenburger, D., and J. Linderman. 1993. Receptors: Models for Binding, Trafficking, and Signaling. Oxford University Press, Oxford, United Kingdom.
17. Andrews, S. S., N. J. Addy, ..., A. P. Arkin. 2010. Detailed simulations of cell biology with Smoldyn 2.1. PLOS Comput. Biol. 6:e1000705.
18. Shoup, D., and A. Szabo. 1982. Role of diffusion in ligand binding to macromolecules and cell-bound receptors. Biophys. J. 40:33-39.
19. Goldstein, B., H. Levine, and D. Torney. 2007. Diffusion limited reactions. SIAM J. Appl. Math. 67:1147-1165. (Pubitemid 47317920)
20. Dushek, O., S. Mueller, . , S. Valitutti. 2008. Effects of intracellular calcium and actin cytoskeleton on TCR mobility measured by fluorescence recovery. PLoS ONE. 3:e3913.
21. Faeder, J. R., M. L. Blinov, and W. S. Hlavacekc. 2009. Rule-based modeling of biochemical systems with BioNetGen. Methods Mol. Biol. 500:113-167.
22. Ciliberto, A., F. Capuani, and J. J. Tyson. 2007. Modeling networks of coupled enzymatic reactions using the total quasi-steady state approximation. PLOS Comput. Biol. 3:e45.
23. Ferrell, Jr., J. E. 1996. Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem. Sci. 21:460-466. (Pubitemid 27018812)
24. Gunawardena, J. 2005. Multisite protein phosphorylation makes a good threshold but can be a poor switch. Proc. Natl. Acad. Sci. USA. 102:14617-14622. (Pubitemid 41457106)
25. Takahashi, K., S. Tanase-Nicola, and P. R. ten Wolde. 2010. Spatiotemporal correlations can drastically change the response of a MAPK pathway. Proc. Natl. Acad. Sci. USA. 107:2473-2478.
26. Adams, J. A. 2001. Kinetic and catalytic mechanisms of protein kinases. Chem. Rev 101:2271-2290. (Pubitemid 35373019)
27. Ubersax, J. A., and J. E. Ferrell, Jr. 2007. Mechanisms of specificity in protein phosphorylation. Nat. Rev Mol. Cell Biol. 8:530-541. (Pubitemid 46985383)
28. Salazar, C., and T. Höfer. 2009. Multisite protein phosphorylationfrom molecular mechanisms to kinetic models. FEBS J. 276:3177-3198.
29. Dushek, O., R. Das, and D. Coombs. 2009. A role for rebinding in rapid and reliable T cell responses to antigen. PLOS Comput. Biol. 5:e1000578.
30. Salazar, C., and T. Höfer. 2007. Versatile regulation of multisite protein phosphorylation by the order of phosphate processing and proteinprotein interactions. FEBS J. 274:1046-1061. (Pubitemid 46204423)
31. Wang, L., Q. Nie, and G. Enciso. 2010. Nonessential sites improve phosphorylation switch. Biophys. J. 99:L41-L43.
32. Liu, X., L. Bardwell, and Q. Nie. 2010. A combination of multisite phosphorylation and substrate sequestration produces switchlike responses. Biophys. J. 98:1396-1407.
33. Lenz, P., and P. S. Swain. 2006. An entropic mechanism to generate highly cooperative and specific binding from protein phosphorylations. Curr. Biol. 16:2150-2155. (Pubitemid 44692097)
34. Ferrell, Jr., J. E., and E. M. Machleder. 1998. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science. 280:895-898. (Pubitemid 28215598)
35. Markevich, N. I., J. B. Hoek, and B. N. Kholodenko. 2004. Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. J. Cell Biol. 164:353-359. (Pubitemid 38174763)
36. Thomson, M., and J. Gunawardena. 2009. Unlimited multistability in multisite phosphorylation systems. Nature. 460:274-277.
37. Sprague, B. L., R. L. Pego, J. G. McNally. 2004. Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys. J. 86:3473-3495. (Pubitemid 38780231)
38. Dushek, O., R. Das, and D. Coombs. 2008. Analysis of membranelocalized binding kinetics with FRAP. Eur. Biophys. J. 37:627-638.
39. Huppa, J. B., M. Axmann, M. M. Davis. 2010. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature. 463:963-967.
40. Barford, D., A. K. Das, and M. P. Egloff. 1998. The structure and mechanism of protein phosphatases: insights into catalysis and regulation. Annu. Rev. Biophys. Biomol. Struct. 27:133-164. (Pubitemid 28286012)
41. Fersht, A. 1999. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. W. H. Freeman, New York.
42. Ramer, S. E., D. G. Winkler, C. T. Walsh. 1991. Purification and initial characterization of the lymphoid-cell protein-tyrosine kinase p56lck from a baculovirus expression system. Proc. Natl. Acad. Sci. USA. 88:6254-6258. (Pubitemid 21914925)
43. Felberg, J., and P. Johnson. 1998. Characterization of recombinant CD45 cytoplasmic domain proteins. Evidence for intramolecular and intermolecular interactions. J. Biol. Chem. 273:17839-17845. (Pubitemid 28355129)
44. van Oers, N. S., B. Tohlen, C. A. Slaughter. 2000. The 21-and 23-kD forms of TCR ζ are generated by specific ITAM phosphorylations. Nat. Immunol. 1:322-328.
45. Samelson, L. E. 2002. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu. Rev. Immunol. 20:371-394. (Pubitemid 34293429)
46. Nag, A., M. I. Monine, . , B. Goldstein. 2009. Aggregation of membrane proteins by cytosolic cross-linkers: theory and simulation of the LAT-Grb2-SOS1 system. Biophys. J. 96:2604-2623.