Distributivity and processivity in multisite phosphorylation can be distinguished through steady-state invariants

Biophysical Journal

Volumn 93, Issue 11, 2007, Pages 3828-3834

  Gunawardena, Jeremy ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATASE; PHOSPHOTRANSFERASE;

ARTICLE; CONCENTRATION (PARAMETERS); MATHEMATICAL ANALYSIS; MEASUREMENT; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; STEADY STATE;

EID: 36849019999     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.110866     Document Type: Article

References (35)

1. Krebs, E. G. 1997. Protein phosphorylation and cellular regulation, I. In Nobel Lectures, Physiology or Medicine 1991-1995. N. Ringertz, editor. World Scientific, Singapore.
2. Manning, G., G. D. Plowman, T. Hunter, and S. Sudarsanam. 2002. Evolution of protein kinase signalling from yeast to man. Trends Biochem. Sci. 27:514-520.
3. Cozzone, A. J. 2005. Role of protein phosphorylation on serine/ threonine and tyrosine in the virulence of bacterial pathogens. J. Mol. Microbiol. Biotechnol. 9:198-213.
4. Cohen, P. 2001. The role of reversible protein phosphorylation in health and disease. Eur. J. Biochem. 268:5001-5010.
5. Stock, A. M., V. L. Robinson, and P. N. Goudreau. 2000. Two component signal transduction. Annu. Rev. Biochem. 69:183-215.
6. Kennelly, P. J. 2003. Archaeal protein kinases and phosphatases: insights from genomics and biochemistry. Biochem. J. 370:373-389.
7. Mann, M., S.-E. Ong, M. Grønberg, H. Steen, O. N. Jensen, and A. Pandey. 2002. Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 20:261-268.
8. Cohen, P. 2000. The regulation of protein function by multisite phosphorylation: a 25 year update. Trends Biochem. Sci. 25:596-601.
9. Holmberg, C. I., S. E. F. Tran, J. E. Eriksson, and L. Sistonen. 2002. Multisite phosphorylation provides sophisticated regulation of transcription factors. Trends Biochem. Sci. 27:619-627.
10. Macek, B., I. Mijakovic, J. V. Olsen, F. Gnad, C. Kumar, P. R. Jensen, and M. Mann. 2007. The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol. Cell. Proteomics. 6:697-707.
11. Rosen, R., D. Becher, K. Buttner, D. Biran, M. Hecker, and E. Z. Ron. 2004. Highly phosphorylated bacterial proteins. Proteomics. 4:3068-3077.
12. Kim, S. Y., and J. E. Ferrell. 2007. Substrate competition as a source of ultrasensitivity in the inactivation of Wee1. Cell. 128:1133-1145.
13. Nakajima, M., K. Imai, H. Ito, T. Nishiwaki, Y. Murayama, H. Iwasaki, T. Oyama, and T. Kondo. 2005. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science. 308:414-415.
14. Huang, C.-Y. F., and J. E. Ferrell. 1996. Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA. 93:10078-10083.
15. Levchenko, A., J. Bruck, 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.
16. 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.
17. Markevich, N. I., J. B. Hoek, and B. N. Kholodenko. 2004. Signalling switches and bistability arising from multisite phosphorylation in protein kinase cascades. J. Cell Biol. 164:353-359.
18. Ortega, F., J. L. Garcés, F. Mas, B. N. Kholodenko, and M. Cascante. 2006. Bistability from double phosphorylation in signal transduction. FEBS J. 273:3915-3926.
19. Reference deleted in press.
20. Hill, T. L. 1985. Cooperativity Theory in Biochemistry: Steady-State and Equilibrium Systems. Springer Series in Molecular Biology. Springer-Verlag, NY.
21. Jeffrey, D. A., M. Springer, D. S. King, and E. K. O'Shea. 2001. Multi-site phosphorylation of Pho4 by the cyclin-CDK Pho80-Pho85 is semi-processive with site preference. J. Mol. Biol. 306:997-1010.
22. Ferrell, J. E., and R. R. Bhatt. 1997. Mechanistic studies of the dual phosphorylation of mitogen-activated protein kinase. J. Biol. Chem. 272:19008-19016.
23. Burack, W. R., and T. W. Sturgill. 1997. The activating dual phosphorylation of MAPK by MEK is nonprocessive. Biochemistry. 36:5929-5933.
24. Pellicena, P., and W. T. Miller. 2001. Processive phosphorylation of p130Cas by Src depends on SH3-polyproline interactions. J. Biol. Chem. 276:28190-28196.
25. Aubol, B. E., S. Chakrabarti, J. Ngo, J. Shaffer, B. Nolen, X.-D. Fu, G. Ghosh, and J. A. Adams. 2003. Processive phosphorylation of alternative splicing factor/splicing factor 2. Proc. Natl. Acad. Sci. USA. 100:12601-12606.
26. Spirin, A. S., V. I. Baranov, L. A. Ryabova, S. Y. Ovodov, and Y. B. Alakhov. 1988. A continuous cell-free translation system capable of producing polypeptides in high yield. Science. 242:1162-1164.
27. Steen, H., J. A. Jebanathirajah, J. Rush, N. Morrice, and M. W. Kirschner. 2005. Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Mol. Cell. Proteomics. 5:172-181.
28. Rape, M., S. K. Reddy, and M. W. Kirschner. 2006. The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell. 124:89-103.
29. Ferrell, 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.
30. Zhao, Y., and Z.-Y. Zhang. 2001. The mechanism of dephosphorylation of extracellular signal-regulated kinase 2 by mitogen-activated protein kinsae phosphatase 3. J. Biol. Chem. 276:32382-32391.
31. Waas, W. F., H.-H. Lo, and K. N. Dalby. 2001. The kinetic mechanism of the dual phosphorylation of the ATF2 transcription factor by p38 mitogen activated protein (MAP) kinase α. J. Biol. Chem. 278:5676-5684.
32. Gunawardena, J. 2005. Multisite protein phosphorylation makes a good threshold but can be a poor switch. Proc. Natl. Acad. Sci. USA. 102:14617-14622.
33. Salazar, C., and T. Höfer. 2007. Versatile regulation of multisite protein phosphorylation by the order of phosphate processing and protein-protein interactions. FEBS J. 274:1046-1060.
34. Harwood, A. J. 2001. Regulation of GSK-3: a cellular multiprocessor. Cell. 105:821-824.
35. Furdui, C. M., E. D. Lew, J. Schlessinger, and K. S. Anderson. 2006. Autophosphorylation of FGFR1 kinase is mediated by a sequential and precisely ordered reaction. Mol. Cell. 21:711-717.