Modeling the mammalian circadian clock: Sensitivity analysis and multiplicity of oscillatory mechanisms

Journal of Theoretical Biology

Volumn 230, Issue 4 SPEC. ISS., 2004, Pages 541-562

  Leloup, Jean Christophe ^a   Goldbeter, Albert ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Circadian rhythms; Computational biology; Model; Sensitivity analysis; Simulations

Indexed keywords

MESSENGER RNA; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK;

CIRCADIAN RHYTHM;

ARTICLE; AUTOREGULATION; CIRCADIAN RHYTHM; COMPUTER SIMULATION; DARKNESS; LIGHT DARK CYCLE; MAMMAL; MATHEMATICAL MODEL; MOLECULAR CLOCK; MOLECULAR MECHANICS; OSCILLATION; PARASOMNIA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SENSITIVITY ANALYSIS; SLEEP WAKING CYCLE; STEADY STATE; SUPRACHIASMATIC NUCLEUS;

MAMMALIA;

EID: 4444301677     PISSN: 00225193     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jtbi.2004.04.040     Document Type: Article

References (74)

1. Allada R., Emery P., Takahashi J.S., Rosbash M. Stopping time. the genetics of fly and mouse circadian clocks Annu. Rev. Neurosci. 24:2001;1091-1119
2. Archer S.N., Robilliard D.L., Skene D.J., Smits M., Williams A., Arendt J., von Schantz M. A length polymorphism in the circadian clock gene Per3 is linked to delayed sleep phase syndrome and extreme diurnal preference. Sleep. 26:2003;413-415
3. Bae K., Lee C., Sidote D., Chuang K.-Y., Edery I. Circadian regulation of a Drosophila homolog of the mammalian Clock gene. PER and TIM function as positive regulators Mol. Cell. Biol. 18:1998;6142-6151
4. Balsalobre A., Damiola F., Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell. 93:1998;929-937
5. Barak S., Tobin E.M., Green R.M., Andronis C., Sugano S. All in good time. the Arabidopsis circadian clock Trends Plant. Sci. 5:2000;517-522
6. Barnes J.W., Tischkau S.A., Barnes J.A., Mitchell J.W., Burgoon P.W., Hickok J.R., Gillette M.U. Requirement of mammalian timeless for circadian rhythmicity. Science. 302:2003;439-442
7. Blau J., Young M.W. Cycling vrille expression is required for a functional Drosophila clock. Cell. 99:1999;661-671
8. Bunger M.K., Wilsbacher L.D., Moran S.M., Clendenin C., Radcliffe L.A., Hogenesch J.B., Simon M.C., Takahashi J.S., Bradfield C.A. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell. 103:2000;1009-1017
9. Ebisawa T., Uchiyama M., Kajimura N., Mishima K., Kamei Y., Katoh M., Watanabe T., Sekimoto M., Shibui K., Kim K., Kudo Y., Ozeki Y., Sugishita M., Toyoshima R., Inoue Y., Yamada N., Nagase T., Ozaki N., Ohara O., Ishida N., Okawa M., Takahashi K., Yamauchi T. Association of structural polymorphisms in the human period3 gene with delayed sleep phase syndrome. EMBO Rep. 2:2001;342-346
10. Engelmann W., Johnsson A., Kobler H.G., Schimmel M. Attenuation of the petal movement rhythm in Kalanchoë with light pulses. Physiol. Plant. 43:1978;68-76
11. Eriksson M.E., Millar A.J. The circadian clock. A plant's best friend in a spinning world. Plant. Physiol. 132:2003;732-738
12. Filipski E., King V.M., Li X., Granda T.G., Mormont M.C., Liu X., Cluastrat B., Hastings M.H., Levi F. Host circadian clock as a control point in tumor progression. J. Natl. Cancer Inst. 94:2002;690-697
13. Forger D.B., Peskin C.S. A detailed predictive model of the mammalian circadian clock. Proc. Natl Acad. Sci. USA. 100:2003;14806-14811
14. Fu L., Pelicano H., Liu J., Huang P., Lee C. The circadian gene period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell. 111:2002;41-50
15. Glossop N.R.J., Lyons L.C., Hardin P.E. Interlocked feedback loops within the Drosophila circadian oscillator. Science. 286:1999;766-768
16. Goldbeter A. A model for circadian oscillations in the Drosophila period protein (PER). Proc. R. Soc. London Ser. B. 261:1995;319-324
17. Goldbeter A. Biochemical Oscillations and Cellular Rhythms. The Molecular Bases of Periodic and Chaotic Behaviour:1996;Cambridge University Press, Cambridge, UK
18. Goldbeter A. Computational approaches to cellular rhythms. Nature. 420:2002;238-245
19. Gonze D., Halloy J., Goldbeter A. Robustness of circadian rhythms with respect to molecular noise. Proc. Natl Acad. Sci. USA. 99:2002;673-678
20. Gonze D., Roussel M., Goldbeter A. A model for the enhancement of fitness in cyanobacteria based on resonance of a circadian oscillator with the external light-dark cycle. J. Theor. Biol. 214:2002;577-597
21. Green R.M., Tobin E.M. Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. Proc. Natl Acad. Sci. USA. 96:1999;4176-4179
22. Hardin P.E., Hall J.C., Rosbash M. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature. 343:1990;536-540
23. Honma S., Honma K. Light-induced uncoupling of multioscillatory circadian system in a diurnal rodent, Asian chipmunk. Am. J. Physiol. 276:1999;R1390-R1396
24. Honma S., Kawamoto T., Takagi Y., Fujimoto K., Sato F., Noshiro M., Kato Y., Honma K.-I. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature. 419:2002;841-844
25. Jewett M.E., Kronauer R.E., Czeisler C.A. Light-induced suppression of endogenous circadian amplitude in humans. Nature. 350:1991;59-62
26. Jewett M.E., Forger D.B., Kronauer R.E. Revised limit cycle oscillator model of human circadian pacemaker. J. Biol. Rhythms. 14:1999;493-499
27. Jones C.R., Campbell S.S., Zone S.E., Cooper F., DeSano A., Murphy P.J., Jones B., Czajkowski L., Ptacek L.J. Familial advanced sleep-phase syndrome. A short-period circadian rhythm variant in humans Nat. Med. 5:1999;1062-1065
28. Kalmus H., Wigglesworth L.A. A. Shock excited systems as models for biological rhythms. Cold Spring Harb. Symp. Quant. Biol. XXV:1960;211-216
29. Kawamoto T., Noshiro M., Sato F., Maemura K., Takeda N., Nagai R., Iwata T., Fujimoto K., Furukawa M., Miyazaki K., Honma S., Honma K., Kato Y. A novel autofeedback loop of Dec1 transcription involved in circadian rhythm regulation. Biochem. Biophys. Res. Commun. 313:2004;117-124
30. Klante G., Steinlechner S. A short red light pulse during dark phase of LD-cycle perturbs the hamster's circadian clock. J. Comp. Physiol. A. 177:1995;775-780
31. Kunz H., Achermann P. Simulation of circadian rhythm generation in the suprachiasmatic nucleus with locally coupled self-sustained oscillators. J. Theor. Biol. 224:2003;63-78
32. Kurosawa G., Mochizuki A., Iwasa Y. Comparative study of circadian clock models, in search of processes promoting oscillation. J. Theor. Biol. 216:2002;193-208
33. Lee K., Loros J.J., Dunlap J.C. Interconnected feedback loops in the Neurospora circadian system. Science. 289:2000;107-110
34. Lee C., Etchegaray J.P., Cagampang F.R., Loudon A.S., Reppert S.M. Posttranslational mechanisms regulate the mammalian circadian clock. Cell. 107:2001;855-867
35. Leloup J.-C., Goldbeter A. A model for circadian rhythms in Drosophila incorporating the formation of a complex between the PER and TIM proteins. J. Biol. Rhythms. 13:1998;70-87
36. Leloup J.-C., Goldbeter A. Modeling the molecular regulatory mechanism of circadian rhythms in Drosophila. BioEssays. 22:2000;83-92
37. Leloup J.-C., Goldbeter A. A molecular explanation for the long-term suppression of circadian rhythms by a single light pulse. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280:2001;R1206-R1212
38. Leloup J.-C., Goldbeter A. Toward a detailed computational model for the mammalian circadian clock. Proc. Natl Acad. Sci. USA. 100:2003;7051-7056
39. Leloup J.-C., Gonze D., Goldbeter A. Limit cycle models for circadian rhythms based on transcriptional regulation in Neurospora and Drosophila. J. Biol. Rhythms. 14:1999;433-448
40. Loros J.J., Dunlap J.C. Genetic and molecular analysis of circadian rhythms in Neurospora. Annu. Rev. Physiol. 63:2001;757-794
41. Merrow M., Brunner M., Roenneberg T. Assignment of circadian function for the Neurospora clock gene frequency. Nature. 399:1999;584-586
42. Minorsky N. Nonlinear Oscillations. 1962;Van Nostrand, Princeton
43. Mori T., Johnson C.H. Circadian programming in cyanobacteria. Semin. Cell. Dev. Biol. 12:2001;271-278
44. Nagano M., Adachi A., Nakahama K., Nakamura T., Tamada M., Meyer-Bernstein E., Sehgal A., Shigeyoshi Y. An abrupt shift in the day/night cycle causes desynchrony in the mammalian circadian center. J. Neurosci. 23:2003;6141-6151
45. Okamura H., Yamaguchi S., Yagita K. Molecular machinery of the circadian clock in mammals. Cell. Tissue Res. 309:2002;47-56
46. Preitner N., Damiola F., Lopez-Molina L., Zakany J., Duboule D., Albrecht U., Schibler U. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell. 110:2002;251-260
47. Reppert S.M., Weaver D.R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 63:2001;647-676
48. Reppert S., Weaver D. Coordination of circadian timing in mammals. Nature. 418:2002;935-941
49. Richardson G.S., Malin H.V. Circadian rhythm sleep disorders. pathophysiology and treatment J. Clin. Neurophysiol. 13:1996;17-31
50. Roden L.C., Carre I.A. The molecular genetics of circadian rhythms in Arabidopsis. Semin. Cell. Dev. Biol. 12:2001;305-315
51. Ruoff P., Vinsjevik M., Monnerjahn C., Rensing L. The Goodwin model. simulating the effect of light pulses on the circadian sporulation rhythm of Neurospora crassa J. Theor. Biol. 209:2001;29-42
52. Schibler U., Ripperger J., Brown S.A. Peripheral circadian oscillators in mammals. time and food J. Biol. Rhythms. 18:2003;250-260
53. Shearman L.P., Sriram S., Weaver D.R., Maywood E.S., Chaves I., Zheng B., Kume K., Lee C.C., van der Horst G.T., Hastings M.H., Reppert S.M. Interacting molecular loops in the mammalian circadian clock. Science. 288:2000;1013-1019
54. Smolen P., Baxter D.A., Byrne J.H. Modeling circadian oscillations with interlocking positive and negative feedback loops. J. Neurosci. 21:2001;6644-6656
55. Smolen P., Hardin P.E., Lo B.S., Baxter D.A., Byrne J.H. Simulation of Drosophila circadian oscillations, mutations, and light responses by a model with VRI, PDP-1, and CLK. Biophys. J. 86:2004;2786-2802
56. Sujino M., Masumoto K.H., Yamaguchi S., van der Horst G.T., Okamura H., Inouye S.T. Suprachiasmatic nucleus grafts restore circadian behavioral rhythms of genetically arrhythmic mice. Curr. Biol. 13:2003;664-668
57. Toh K.L., Jones C.R., He Y., Eide E.J., Hinz W.A., Virshup D.M., Ptacek L.J., Fu Y.-H. An hPer2 phosphorylation site mutation in familial advanced sleep-phase syndrome. Science. 291:2001;1040-1043
58. Tyson J.J., Novak B. Regulation of the eukaryotic cell cycle. molecular antagonism, hysteresis, and irreversible transitions J. Theor. Biol. 210:2001;249-263
59. Tyson J.J., Hong C.I., Thron C.D., Novak B. A simple model of circadian rhythms based on dimerization and proteolysis of PER and TIM. Biophys. J. 77:1999;2411-2417
60. Ueda H.R., Hagiwara M., Kitano H. Robust oscillations within the interlocked feedback model of Drosophila circadian rhythm. J. Theor. Biol. 210:2001;401-406
61. van der Horst G.T., Muijtjens M., Kobayashi K., Takano R., Kanno S., Takao M., de Wit J., Verkerk A., Eker A.P., van Leenen D., Buijs R., Bootsma D., Hoeijmakers J.H., Yasui A. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature. 398:1999;627-630
62. 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. 18:2003;125-133
63. Williams J.A., Sehgal A. Molecular components of the circadian system in Drosophila. Annu. Rev. Physiol. 63:2001;729-755
64. Winfree A.T. Biological rhythms and the behavior of populations of coupled oscillators. J. Theor. Biol. 16:1967;15-42
65. Winfree A.T. Integrated view of resetting a circadian clock. J. Theor. Biol. 28:1970;327-374
66. Winfree A.T. The investigation of oscillatory processes by perturbation experiments. Chance B., Pye E.K., Ghosh A.K., Hess B. Biological and Biochemical Oscillators. 1973;461-502 Academic Press, New York
67. Winfree, A.T., 1980. The Geometry of Biological Time. 2nd Edition, Springer, New York, 2001.
68. Yoo S.H., Yamazaki S., Lowrey P.L., Shimomura K., Ko C.H., Buhr E.D., Siepka S.M., Hong H.K., Oh W.J., Yoo O.J., Menaker M., Takahashi J.S. PERIOD2. LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues Proc. Natl Acad. Sci. USA. 101:2004;5339-5346
69. Yoshii T., Sakamoto M., Tomioka K. A temperature-dependent timing mechanism is involved in the circadian system that drives locomotor rhythms in the fruit fly Drosophila melanogaster. Zool. Sci. 19:2002;841-850
70. Young M.W., Kay S.A. Time zones. a comparative genetics of circadian clocks Nat. Rev. Genet. 2:2001;702-715
71. Yu W., Nomura M., Ikeda M. Interactivating feedback loops within the mammalian clock. BMAL1 is negatively autoregulated and upregulated by CRY1, CRY2, and PER2 Biochem. Biophys. Res. Com. 290:2002;933-941
72. Zeng H., Qian Z., Myers M.P., Rosbash M. A light-entrainment mechanism for the Drosophila circadian clock. Nature. 380:1996;129-135
73. Zheng B., Albrecht U., Kaasik K., Sage M., Lu W., Vaishnav S., Li Q., Sun Z.S., Eichele G., Bradley A., Lee C.C. Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell. 105:2001;683-694
74. Zylka M.J., Shearman L.P., Weaver D.R., Reppert S.M. Three period homologs in mammals. differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain Neuron. 20:1998;1103-1110