A combination of multisite phosphorylation and substrate sequestration produces switchlike responses

Biophysical Journal

Volumn 98, Issue 8, 2010, Pages 1396-1407

  Liu, Xinfeng ^a   Bardwell, Lee ^b   Nie, Qing ^b  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77951639384     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.12.4307     Document Type: Article

References (48)

1. Manning, G., D. B. Whyte,..., S. Sudarsanam. 2002. The protein kinase complement of the human genome. Science. 298:1912-1934.
2. Mann, M., S. E. Ong, ..., A. Pandey. 2002. Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 20:261-268. (Pubitemid 34451062)
3. Barford, D., S. H. Hu, and L. N. Johnson. 1991. Structural mechanism for glycogen Phosphorylase control by phosphorylation and AMP. J. Mol. Biol. 218:233-260. (Pubitemid 121003342)
4. Kholodenko, B. N. 2006. Cell-signaling dynamics in time and space. Nat. Rev. Mol. Cell Biol. 7:165-176.
5. Shacter-Noiman, E., P. B. Chock, and E. R. Stadtman. 1983. Protein phosphorylation as a regulatory device. Philos. Trans. R. Soc. Land., B. 302:157-166.
6. 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.
7. Brown, G. C., J. B. Hoek, and B. N. Kholodenko. 1997. Why do protein kinase cascades have more than one level? Trends Biochem. Sci. 22:288-289.
8. Ferrell, Jr., J. E. 1996. Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switchlike outputs. Biochem. Sci. 21:460-466.
9. Hooshangi, S., S. Thiberge, and R. Weiss. 2005. Ultrasensitivity and noise propagation in a synthetic transcriptional cascade. Proc. Natl. Acad. Sci. USA. 102:3581-3586.
10. Pomerening, J. R. 2008. Uncovering mechanisms of bistability in biological systems. Curr. Opin. Biotechnol. 19:381-388.
11. Buchler, N. E., and M. Louis. 2008. Molecular titration, and ultrasensitivity in regulatory networks. J. Mol. Biol. 384; 1106-1119.
12. Lapidus, S., B. Han, and J. Wang. 2008. Intrinsic noise, dissipation cost, and robustness of cellular networks: the underlying energy landscape of MAPK signal transduction, Proc. Natl. Acad. Sci. USA. 105: 6039-6044.
13. Meinke, M. H., J. S. Bishop, and R. D. Edstrom. 1986. Zero-order ultrasensitivity in the regulation of glycogen Phosphorylase. Proc. Natl. Acad. Sci. USA. 83:2865-2868.
14. Salazar, C., and T. Höfer. 2003. Allosteric regulation of the transcription factor NFAT1 by multiple phosphorylation sites: a mathematical analysis. J. Mol. Biol. 327:31-45.
15. Nash, P., X. Tang, ..., M. Tyers. 2001, Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature. 414:514-521.
16. Huang, C. Y., and J. E. J. Ferrell, Jr. 1996. Ultrasensitivity in the mitogen-activated protein, kinase cascade. Proc. Natl. Acad. Sci. USA. 93:10078-10083.
17. Hardie, D. G., I. P. Salt, ..., S. P. Davies. 1999. AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem. J. 338:717-722.
18. 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.
19. Bagowski, C. P., J. Besser, ..., J. E. Ferrell. 2003. The JNK cascade as a biochemical switch in mammalian cells. Ultrasensitive and all-or-none responses. Curr. Biol. 13:315-320.
20. 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.
21. Serber, Z., and J. E. Ferrell, Jr. 2007. Tuning bulk electrostatics to regulate protein function. Cell. 128:441-444.
22. 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)
23. Ortega, F., J. L. Garces, ..., M. Cascante. 2006. Bistability from double phosphorylation in signal transduction. Kinetic and structural requirements. FEBS J. 273:3915-3926.
24. Blenis, J., and M. D. Resh. 1993. Subcellular localization specified by protein acylation and phosphorylation. Curr. Opin. Cell Biol. 5:984-989. (Pubitemid 23340505)
25. Karin, M. 1994. Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr. Opin. Cell Biol. 6:415-424.
26. Whitmarsh, A. J., and R. J. Davis. 2000. Regulation of transcription factor function by phosphorylation. Cell. Mol. Life Sci. 57:1172-1183. (Pubitemid 30663475)
27. Cyert, M. S. 2001, Regulation of nuclear localization during signaling. J. Biol. Chem. 276:20805-20808.
28. Pawson, T. 2004. Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell. 116:191-203. (Pubitemid 38167312)
29. Van Der Heide, L. P., M. F. Hoekman, and M. P. Smidt. 2004. The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem. J. 380:297-309. (Pubitemid 38788101)
30. Ferrell, Jr., J. E. 1998. How regulated protein translocation can produce switchlike responses. Trends Biochem. Sci. 23:461-465.
31. Kondoh, K., S. Torii, and E. Nishida. 2005. Control of MAP kinase signaling to the nucleus. Chromosoma. 114:86-91. (Pubitemid 41030971)
32. Bridges, D., and G. B. Moorhead. 2005. 14-3-3 proteins: a number of functions for a numbered protein. Sci. STKE. 2005:re10.
33. Blüthgen, N., F. J. Bruggeman, ..., B. N. Kholodenko. 2006. Effects of sequestration, on signal transduction cascades. FEBS J. 273: 895-906.
34. Chickarmane, V., B. N. Kholodenko, and H. M. Sauro. 2007. Oscillatory dynamics arising from competitive inhibition and multisite phosphorylation. J. Theor. Biol. 244:68-76.
35. Legewie, S., B. Schoeberl, ..., H. Herzel. 2007. Competing docking interactions can bring about bistability in the MAPK cascade. Biophys. J. 93:2279-2288.
36. Kirschner, M., and J. Gerhart. 1998. Evolvability. Proc.Natl.Acad. Sci. USA. 95:8420-8427.
37. Ptashne, M., and A. Gann. 2002. Genes and Signals. Cold Spring Harbor Laboratory Press, New York.
38. Bhattacharyya, R. P., A. Reményi, ..., W. A. Lim. 2006. Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu. Rev. Biochem. 75:655-680.
39. Bardwell, L. 2008. Signal transduction; turning a switch into a rheostat. Curr. Biol. 18:R910-R912.
40. Strickfaden, S. C., M. J. Winters, ..., P. M. Pryciak. 2007. A mechanism for cell-cycle regulation of MAP kinase signaling in a yeast differentiation pathway. Cell. 128:519-531. (Pubitemid 46198890)
41. Flatauer, L. J., S. F. Zadeh, and L. Bardwell, 2005. Mitogen-activated protein, kinases with distinct requirements for Ste5 scaffolding influence signaling specificity in Saccharomyces cerevisiae. Mol. Cell. Biol. 25:1793-1803.
42. Whitmarsh, A. J., and R. J. Davis. 1998. Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem. Sci. 23:481-485.
43. Kusari, A. B., D. M. Molina, ..., L. Bardwell. 2004. A conserved protein interaction network involving the yeast MAP kinases Fus3 and Kssl, J. Cell Biol. 164:267-277.
44. 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.
45. Salazar, C., and T. Höfer. 2009. Multisite protein phosphorylationfrom, molecular mechanisms to kinetic models. FEBS J. 276:3177-3198.
46. Levchenko, A., J. Brück, and P. W. Sternberg. 2000. Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc. Natl. Acad. Sci. USA. 97:5818-5823.
47. Takahashi, S., and P. M. Pryciak. 2008. Membrane localization of scaffold proteins promotes graded signaling in the yeast MAP kinase cascade. Curr. Biol. 18:1184-1191.
48. Holt, J. M., and G. K. Ackers. 1995. The pathway of allosteric control as revealed by hemoglobin intermediate states. FASEB J. 9: 210-218.