A Design Principle for a Posttranslational Biochemical Oscillator

Cell Reports

Volumn 2, Issue 4, 2012, Pages 938-950

  Jolley, Craig C ^a   Ode, Koji L ^b   Ueda, Hiroki R ^a,b,c,d  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b RIKEN   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATASE; PHOSPHOTRANSFERASE;

ARTICLE; CIRCADIAN RHYTHM; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME MODIFICATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; OSCILLATION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROCESSING; STOCHASTIC MODEL; TEMPERATURE SENSITIVITY;

BIOLOGICAL CLOCKS; CIRCADIAN CLOCKS; MODELS, THEORETICAL; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN KINASES; TEMPERATURE;

EID: 84868139341     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.09.006     Document Type: Article

References (73)

1. Akashi M., Tsuchiya Y., Yoshino T., Nishida E. Control of intracellular dynamics of mammalian period proteins by casein kinase I epsilon (CKIepsilon) and CKIdelta in cultured cells. Mol. Cell. Biol. 2002, 22:1693-1703.
2. 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, 273:895-906.
3. Camacho F., Cilio M., Guo Y., Virshup D.M., Patel K., Khorkova O., Styren S., Morse B., Yao Z., Keesler G.A. Human casein kinase Idelta phosphorylation of human circadian clock proteins period 1 and 2. FEBS Lett. 2001, 489:159-165.
4. Chen Z., Yoo S.H., Park Y.S., Kim K.H., Wei S., Buhr E., Ye Z.Y., Pan H.L., Takahashi J.S. Identification of diverse modulators of central and peripheral circadian clocks by high-throughput chemical screening. Proc. Natl. Acad. Sci. USA 2012, 109:101-106.
5. Chickarmane V., Kholodenko B.N., Sauro H.M. Oscillatory dynamics arising from competitive inhibition and multisite phosphorylation. J. Theor. Biol. 2007, 244:68-76.
6. Clodong S., Dühring U., Kronk L., Wilde A., Axmann I., Herzel H., Kollmann M. Functioning and robustness of a bacterial circadian clock. Mol. Syst. Biol. 2007, 3:90.
7. Conrad E., Mayo A.E., Ninfa A.J., Forger D.B. Rate constants rather than biochemical mechanism determine behaviour of genetic clocks. J. R. Soc. Interface 2008, 5(Suppl 1):S9-S15.
8. Dibner C., Sage D., Unser M., Bauer C., d'Eysmond T., Naef F., Schibler U. Circadian gene expression is resilient to large fluctuations in overall transcription rates. EMBO J. 2009, 28:123-134.
9. Dibner C., Schibler U., Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 2010, 72:517-549.
10. Dunlap J.C. Molecular bases for circadian clocks. Cell 1999, 96:271-290.
11. Dunlap J.C., Loros J.J., Decoursey P.J. Chronobiology: Biological Timekeeping, First Edition 2003, Sinauer Associates, Sunderland, MA.
12. Fan Y., Hida A., Anderson D.A., Izumo M., Johnson C.H. Cycling of CRYPTOCHROME proteins is not necessary for circadian-clock function in mammalian fibroblasts. Curr. Biol. 2007, 17:1091-1100.
13. Ferrell J.E., Tsai T.Y., Yang Q. Modeling the cell cycle: why do certain circuits oscillate?. Cell 2011, 144:874-885.
14. Flotow H., Graves P.R., Wang A.Q., Fiol C.J., Roeske R.W., Roach P.J. Phosphate groups as substrate determinants for casein kinase I action. J. Biol. Chem. 1990, 265:14264-14269.
15. Gallego M., Virshup D.M. Post-translational modifications regulate the ticking of the circadian clock. Nat. Rev. Mol. Cell Biol. 2007, 8:139-148.
16. Gallego M., Eide E.J., Woolf M.F., Virshup D.M., Forger D.B. An opposite role for tau in circadian rhythms revealed by mathematical modeling. Proc. Natl. Acad. Sci. USA 2006, 103:10618-10623.
17. Gallego M., Kang H., Virshup D.M. Protein phosphatase 1 regulates the stability of the circadian protein PER2. Biochem. J. 2006, 399:169-175.
18. Gekakis N., Staknis D., Nguyen H.B., Davis F.C., Wilsbacher L.D., King D.P., Takahashi J.S., Weitz C.J. Role of the CLOCK protein in the mammalian circadian mechanism. Science 1998, 280:1564-1569.
19. Gillespie D.T. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 1977, 81:2340-2361.
20. Griffin E.A., Staknis D., Weitz C.J. Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science 1999, 286:768-771.
21. Guantes R., Poyatos J.F. Dynamical principles of two-component genetic oscillators. PLoS Comput. Biol. 2006, 2:e30.
22. Hastings J.W., Sweeney B.M. On the mechanism of temperature independence in a biological clock. Proc. Natl. Acad. Sci. USA 1957, 43:804-811.
23. Hatakeyama T.S., Kaneko K. Generic temperature compensation of biological clocks by autonomous regulation of catalyst concentration. Proc. Natl. Acad. Sci. USA 2012, 109:8109-8114.
24. Hirota T., Lewis W.G., Liu A.C., Lee J.W., Schultz P.G., Kay S.A. A chemical biology approach reveals period shortening of the mammalian circadian clock by specific inhibition of GSK-3beta. Proc. Natl. Acad. Sci. USA 2008, 105:20746-20751.
25. Hogenesch J.B., Ueda H.R. Understanding systems-level properties: timely stories from the study of clocks. Nat. Rev. Genet. 2011, 12:407-416.
26. Huang C.Y., Ferrell J.E. Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 1996, 93:10078-10083.
27. Isojima Y., Nakajima M., Ukai H., Fujishima H., Yamada R.G., Masumoto K.H., Kiuchi R., Ishida M., Ukai-Tadenuma M., Minami Y., et al. CKIepsilon/δ-dependent phosphorylation is a temperature-insensitive, period-determining process in the mammalian circadian clock. Proc. Natl. Acad. Sci. USA 2009, 106:15744-15749.
28. Johnson C.H., Mori T., Xu Y. A cyanobacterial circadian clockwork. Curr. Biol. 2008, 18:R816-R825.
29. Kholodenko B.N. Negative feedback and ultrasensitivity can bring about oscillations in the mitogen-activated protein kinase cascades. Eur. J. Biochem. 2000, 267:1583-1588.
30. Kholodenko B.N. Cell-signalling dynamics in time and space. Nat. Rev. Mol. Cell Biol. 2006, 7:165-176.
31. Kume K., Zylka M.J., Sriram S., Shearman L.P., Weaver D.R., Jin X., Maywood E.S., Hastings M.H., Reppert S.M. mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 1999, 98:193-205.
32. Lee C., Etchegaray J.P., Cagampang F.R., Loudon A.S., Reppert S.M. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 2001, 107:855-867.
33. Lee C., Weaver D.R., Reppert S.M. Direct association between mouse PERIOD and CKIepsilon is critical for a functioning circadian clock. Mol. Cell. Biol. 2004, 24:584-594.
34. Lee H.M., Chen R., Kim H., Etchegaray J.P., Weaver D.R., Lee C. The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1. Proc. Natl. Acad. Sci. USA 2011, 108:16451-16456.
35. Legewie S., Blüthgen N., Herzel H. Mathematical modeling identifies inhibitors of apoptosis as mediators of positive feedback and bistability. PLoS Comput. Biol. 2006, 2:e120.
36. Legewie S., Schoeberl B., Blüthgen N., Herzel H. Competing docking interactions can bring about bistability in the MAPK cascade. Biophys. J. 2007, 93:2279-2288.
37. Liu P., Kevrekidis I.G., Shvartsman S.Y. Substrate-dependent control of ERK phosphorylation can lead to oscillations. Biophys. J. 2011, 101:2572-2581.
38. Lowrey P.L., Shimomura K., Antoch M.P., Yamazaki S., Zemenides P.D., Ralph M.R., Menaker M., Takahashi J.S. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 2000, 288:483-492.
39. Maier B., Wendt S., Vanselow J.T., Wallach T., Reischl S., Oehmke S., Schlosser A., Kramer A. A large-scale functional RNAi screen reveals a role for CK2 in the mammalian circadian clock. Genes Dev. 2009, 23:708-718.
40. 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, 164:353-359.
41. Meng Q.J., Logunova L., Maywood E.S., Gallego M., Lebiecki J., Brown T.M., Sládek M., Semikhodskii A.S., Glossop N.R., Piggins H.D., et al. Setting clock speed in mammals: the CK1 epsilon tau mutation in mice accelerates circadian pacemakers by selectively destabilizing PERIOD proteins. Neuron 2008, 58:78-88.
42. Meng Q.J., Maywood E.S., Bechtold D.A., Lu W.Q., Li J., Gibbs J.E., Dupré S.M., Chesham J.E., Rajamohan F., Knafels J., et al. Entrainment of disrupted circadian behavior through inhibition of casein kinase 1 (CK1) enzymes. Proc. Natl. Acad. Sci. USA 2010, 107:15240-15245.
43. Nakajima M., Imai K., Ito H., Nishiwaki T., Murayama Y., Iwasaki H., Oyama T., Kondo T. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 2005, 308:414-415.
44. Nishiwaki T., Satomi Y., Kitayama Y., Terauchi K., Kiyohara R., Takao T., Kondo T. A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria. EMBO J. 2007, 26:4029-4037.
45. Novák B., Tyson J.J. Design principles of biochemical oscillators. Nat. Rev. Mol. Cell Biol. 2008, 9:981-991.
46. O'Neill J.S., Reddy A.B. Circadian clocks in human red blood cells. Nature 2011, 469:498-503.
47. Okamura H., Miyake S., Sumi Y., Yamaguchi S., Yasui A., Muijtjens M., Hoeijmakers J.H., van der Horst G.T. Photic induction of mPer1 and mPer2 in cry-deficient mice lacking a biological clock. Science 1999, 286:2531-2534.
48. Partch C.L., Shields K.F., Thompson C.L., Selby C.P., Sancar A. Posttranslational regulation of the mammalian circadian clock by cryptochrome and protein phosphatase 5. Proc. Natl. Acad. Sci. USA 2006, 103:10467-10472.
49. Pittendrigh C.S. On temperature independence in the clock system controlling emergence time in Drosophila. Proc. Natl. Acad. Sci. USA 1954, 40:1018-1029.
50. Plimpton, S., Battaile, C., Chandross, M., Holm, L., Thompson, A., Tikare, V., Wagner, G., Webb, E., Zhou, X., Garcia-Cardona, C., et al. (2009). Crossing the mesoscale no-man's land via parallel kinetic Monte Carlo. Sandia Report SAND2009-6226.
51. Qiao L., Nachbar R.B., Kevrekidis I.G., Shvartsman S.Y. Bistability and oscillations in the Huang-Ferrell model of MAPK signaling. PLoS Comput. Biol. 2007, 3:1819-1826.
52. Reppert S.M., Weaver D.R. Coordination of circadian timing in mammals. Nature 2002, 418:935-941.
53. Rust M.J., Markson J.S., Lane W.S., Fisher D.S., O'Shea E.K. Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 2007, 318:809-812.
54. Sato T.K., Yamada R.G., Ukai H., Baggs J.E., Miraglia L.J., Kobayashi T.J., Welsh D.K., Kay S.A., Ueda H.R., Hogenesch J.B. Feedback repression is required for mammalian circadian clock function. Nat. Genet. 2006, 38:312-319.
55. Schlosser A., Vanselow J.T., Kramer A. Mapping of phosphorylation sites by a multi-protease approach with specific phosphopeptide enrichment and NanoLC-MS/MS analysis. Anal. Chem. 2005, 77:5243-5250.
56. Schmutz I., Wendt S., Schnell A., Kramer A., Mansuy I.M., Albrecht U. Protein phosphatase 1 (PP1) is a post-translational regulator of the mammalian circadian clock. PLoS ONE 2011, 6:e21325.
57. Shankaran H., Ippolito D.L., Chrisler W.B., Resat H., Bollinger N., Opresko L.K., Wiley H.S. Rapid and sustained nuclear-cytoplasmic ERK oscillations induced by epidermal growth factor. Mol. Syst. Biol. 2009, 5:332.
58. Strogatz S.H. Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering 1994, Addison-Wesley, Reading, MA.
59. Takahashi J.S., Hong H.K., Ko C.H., McDearmon E.L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 2008, 9:764-775.
60. Takano A., Shimizu K., Kani S., Buijs R.M., Okada M., Nagai K. Cloning and characterization of rat casein kinase 1epsilon. FEBS Lett. 2000, 477:106-112.
61. Thomson M., Gunawardena J. Unlimited multistability in multisite phosphorylation systems. Nature 2009, 460:274-277.
62. Toh K.L., Jones C.R., He Y., Eide E.J., Hinz W.A., Virshup D.M., Ptácek L.J., Fu Y.H. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 2001, 291:1040-1043.
63. Tsuchiya Y., Akashi M., Matsuda M., Goto K., Miyata Y., Node K., Nishida E. Involvement of the protein kinase CK2 in the regulation of mammalian circadian rhythms. Sci. Signal. 2009, 2:ra26.
64. Ueda H.R., Hayashi S., Chen W., Sano M., Machida M., Shigeyoshi Y., Iino M., Hashimoto S. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genet. 2005, 37:187-192.
65. Ukai-Tadenuma M., Yamada R.G., Xu H., Ripperger J.A., Liu A.C., Ueda H.R. Delay in feedback repression by cryptochrome 1 is required for circadian clock function. Cell 2011, 144:268-281.
66. van Zon J.S., Lubensky D.K., Altena P.R., ten Wolde P.R. An allosteric model of circadian KaiC phosphorylation. Proc. Natl. Acad. Sci. USA 2007, 104:7420-7425.
67. Vanselow K., Vanselow J.T., Westermark P.O., Reischl S., Maier B., Korte T., Herrmann A., Herzel H., Schlosser A., Kramer A. Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev. 2006, 20:2660-2672.
68. Vielhaber E., Eide E., Rivers A., Gao Z.H., Virshup D.M. Nuclear entry of the circadian regulator mPER1 is controlled by mammalian casein kinase I epsilon. Mol. Cell. Biol. 2000, 20:4888-4899.
69. von Gall C., Noton E., Lee C., Weaver D.R. Light does not degrade the constitutively expressed BMAL1 protein in the mouse suprachiasmatic nucleus. Eur. J. Neurosci. 2003, 18:125-133.
70. Walton K.M., Fisher K., Rubitski D., Marconi M., Meng Q.J., Sládek M., Adams J., Bass M., Chandrasekaran R., Butler T., et al. Selective inhibition of casein kinase 1 epsilon minimally alters circadian clock period. J. Pharmacol. Exp. Ther. 2009, 330:430-439.
71. Xu Y., Padiath Q.S., Shapiro R.E., Jones C.R., Wu S.C., Saigoh N., Saigoh K., Ptácek L.J., Fu Y.H. Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature 2005, 434:640-644.
72. Xu Y., Toh K.L., Jones C.R., Shin J.Y., Fu Y.H., Ptácek L.J. Modeling of a human circadian mutation yields insights into clock regulation by PER2. Cell 2007, 128:59-70.
73. Young M.W., Kay S.A. Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2001, 2:702-715.