Exact analysis of intrinsic qualitative features of phosphorelays using mathematical models

Journal of Theoretical Biology

Volumn 300, Issue , 2012, Pages 7-18

  Knudsen, Michael ^a   Feliu, Elisenda ^b   Wiuf, Carsten ^b  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Chemical reaction network; Mass action; Steady state; Stimulus response; Two component system

Indexed keywords

CHEMICAL ALTERATION; CHEMICAL CUE; CHEMOTAXIS; COMPUTER SIMULATION; NETWORK ANALYSIS; NUMERICAL MODEL; OSMOREGULATION; PROKARYOTE; QUALITATIVE ANALYSIS; REACTION KINETICS; STEADY-STATE EQUILIBRIUM; VIRULENCE;

ARTICLE; CELL FUNCTION; CELL KINETICS; CHEMICAL REACTION; CHEMICAL REACTION KINETICS; CONCENTRATION (PARAMETERS); MASS ACTION; MATHEMATICAL MODEL; NONHUMAN; PHOSPHORELAY; PHOSPHORYLATION; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SIMULATION; STEADY STATE; STIMULATION; STIMULUS RESPONSE;

MODELS, BIOLOGICAL; PHOSPHATES; PHOSPHORYLATION; PROKARYOTIC CELLS; PROTEIN KINASES; SIGNAL TRANSDUCTION; SYSTEMS THEORY;

PROKARYOTA;

EID: 84858163290     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2012.01.007     Document Type: Article

References (51)

1. Angeli D., de Leenheer P., Sontag E.D. A Petri net approach to the study of persistence in chemical reaction networks. Math. Biosci. 2007, 210(2):598-618.
2. Angeli D., de Leenheer P., Sontag E. Graph-theoretic characterizations of monotonicity of chemical networks in reaction coordinates. J. Math. Biol. 2010, 61(4):581-616.
3. Appleby J., Parkinson J. Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 1996, 86:845-848.
4. Banaji M., Craciun G. Graph-theoretic criteria for injectivity and unique equilibria in general chemical reaction systems. Adv. Appl. Math. 2010, 44(2):168-184.
5. Barkai N., Leibler S. Robustness in simple biochemical networks. Nature 1997, 387(6636):913-917.
6. Batchelor E., Goulian M. Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. Proc. Natl. Acad. Sci. USA 2003, 100(2):691-696.
7. Blüthgen N., Bruggeman F.J., Legewie S., Herzel H., Westerhoff H.V., Kholodenko B.N. Effects of sequestration on signal transduction cascades. FEBS J. 2006, 273(5):895-906.
8. Burbulys D., Trach K.A., Hoch J.A. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 1991, 64(3):545-552.
9. Chang C., Stewart R.C. The two-component system. Regulation of diverse signaling pathways in prokaryotes and eukaryotes. Plant Physiol. 1998, 117(3):723-731.
10. Cohen P. The regulation of protein function by multisite phosphorylation-a 25 year update. Trends Biochem. Sci. 2000, 25(12):596-601.
11. Conradi C., Flockerzi D., Raisch J. Multistationarity in the activation of a MAPK: parametrizing the relevant region in parameter space. Math. Biosci. 2008, 211(1):105-131.
12. Cotter P.A., Jones A.M. Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol 2003, 11(8):367-373.
13. Csikász-Nagy A., Cardelli L., Soyer O.S. Response dynamics of phosphorelays suggest their potential utility in cell signalling. J. Roy. Soc. Interface 2011, 8(57):480-488.
14. Feliu, E., Wiuf, C., 2011. Variable elimination in chemical reaction networks with mass action kinetics. arXiv:1109.1505v1.
15. Feliu, E., Wiuf, C., Enzyme sharing as a cause of multistationarity in signaling systems. J. Roy. Soc. Interface, , in press. http://10.1098/rsif.2011.0664.
16. Feliu E., Knudsen M., Andersen L.N., Wiuf C. An algebraic approach to signaling cascades with n layers. Bull. Math. Biol. 2012, 74:45-72.
17. Feliu E., Knudsen M., Wiuf C. Signaling cascades: consequences of varying substrate and phosphatase levels. Adv. Exp. Med. Biol. 2012, 736(1):81-94.
18. Fujita M., Losick R. Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev. 2005, 19(18):2236-2244.
19. Goldbeter A., Koshland D.E. An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. USA 1981, 78(11):6840-6844.
20. Goldbeter A., Koshland D.E. Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero-order and multistep effects. J. Biol. Chem. 1984, 259(23):14441-14447.
21. Gunawardena J. Multisite protein phosphorylation makes a good threshold but can be a poor switch. Proc. Natl. Acad. Sci. USA 2005, 102(41):14617-14622.
22. Gunawardena J. Distributivity and processivity in multisite phosphorylation can be distinguished through steady-state invariants. Biophys. J. 2007, 93(11):3828-3834.
23. Gunawardena J. Biological systems theory. Science 2010, 328(5978):581-582.
24. Hoch J.A. Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. Ann. Rev. Microbiol. 1993, 47:441-465.
25. Huang C.Y., Ferrell J.E. Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 1996, 93(19):10078-10083.
26. Kapuy O., Barik D., Sananes M.R.D., Tyson J.J., Novák B. Bistability by multiple phosphorylation of regulatory proteins. Prog. Biophys. Mol. Biol. 2009, 100(1-3):47-56.
27. Kim J.-R., Cho K.-H. The multi-step phosphorelay mechanism of unorthodox two-component systems in E. coli realizes ultrasensitivity to stimuli while maintaining robustness to noises. Comput. Biol. Chem. 2006, 30(6):438-444.
28. Li F., Long T., Lu Y., Ouyang Q., Tang C. The yeast cell-cycle network is robustly designed. Proc. Natl. Acad. Sci. USA 2004, 101(14):4781-4786.
29. Maeda T., Wurgler-Murphy S.M., Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 1994, 369(6477):242-245.
30. Manrai A.K., Gunawardena J. The geometry of multisite phosphorylation. Biophys. J. 2008, 95(12):5533-5543.
31. Markevich N.I., Hoek J.B., Kholodenko B.N. Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. J. Cell Biol. 2004, 164(3):353-359.
32. Mizuno T. Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res. 1997, 4:161-168.
33. Molle V., Fujita M., Jensen S.T., Eichenberger P., González-Pastor J.E., Liu J.S., Losick R. The Spo0A regulon of Bacillus subtilis. Mol. Microbiol. 2003, 50(5):1683-1701.
34. Ohlsen K.L., Grimsley J.K., Hoch J.A. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc. Natl. Acad. Sci. USA 1994, 91(5):1756-1760.
35. Perego M., Hoch J.A. Protein aspartate phosphatases control the output of two-component signal transduction systems. Trends Genet. 1996, 12(3):97-101.
36. Perraud A.L., Weiss V., Gross R. Signalling pathways in two-component phosphorelay systems. Trends Microbiol. 1999, 7(3):115-120.
37. Posas F., Wurgler-Murphy S.M., Maeda T., Witten E.A., Thai T.C., Saito H. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 1996, 86(6):865-875.
38. Russo F., Silhavy T. EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J. Mol. Biol. 1991, 222:567-580.
39. Saito H. Histidine phosphorylation and two-component signaling in eukaryotic cells. Chem. Rev. 2001, 101(8):2497-2509.
40. Salazar C. Multisite protein phosphorylation-from molecular mechanisms to kinetic models. FEBS J. 2009, 276:3177-3198.
41. Salazar C., Höfer T. Versatile regulation of multisite protein phosphorylation by the order of phosphate processing and protein-protein interactions. FEBS J. 2007, 274(4):1046-1061.
42. Shinar G., Feinberg M. Structural sources of robustness in biochemical reaction networks. Science 2010, 327(5971):1389-1391.
43. Shinar G., Milo R., Martínez M.R., Alon U. Input-output robustness in simple bacterial signaling systems. Proc. Natl. Acad. Sci. USA 2007, 104(50):19931-19935.
44. Stock A.M., Robinson V.L., Goudreau P.N. Two-component signal transduction. Ann. Rev. Biochem. 2000, 69:183-215.
45. Thomson M., Gunawardena J. Unlimited multistability in multisite phosphorylation systems. Nature 2009, 460(7252):274-277.
46. Thomson M., Gunawardena J. The rational parameterisation theorem for multisite post-translational modification systems. J. Theor. Biol. 2009, 261(4):626-636.
47. Uhl M., Miller J. Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J. 1996, 15(5):1028-1036.
48. Ventura A.C., Sepulchre J.-A., Merajver S.D. A hidden feedback in signaling cascades is revealed. PLoS Comput. Biol. 2008, 4(3):e1000041.
49. Wang L., Sontag E.D. On the number of steady states in a multiple futile cycle. J. Math. Biol. 2007, 57(1):29-52.
50. West A.H., Stock A.M. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 2001, 26(6):369-376.
51. Zhang W., Shi L. Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases. Microbiology 2005, 151:2159-2173.