Robustness from flexibility in the fungal circadian clock

BMC Systems Biology

Volumn 4, Issue , 2010, Pages

  Akman, Ozgur E ^a,b,c   Rand, David A ^b   Brown, Paul E ^b   Millar, Andrew J ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; NEUROSPORA;

FRQ PROTEIN, NEUROSPORA CRASSA; FUNGAL PROTEIN;

ARTICLE; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; COMPUTER SIMULATION; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; HOMEOSTASIS; METABOLISM; NEUROSPORA CRASSA; PHOTOPERIODICITY; PHYSIOLOGY;

BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION; HOMEOSTASIS; MODELS, BIOLOGICAL; NEUROSPORA CRASSA; PHOTOPERIOD;

EID: 77955381783     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-4-88     Document Type: Article

References (65)

1. Dunlap JC, Loros JL, DeCoursey PJ. Chronobiology: Biological TimeKeeping 2003, Sunderland, MA, Sinauer.
2. Young MW, Kay SA. Time zones: a comparative genetics of circadian clocks. Nat Rev Genet 2001, 2(9):702-15. 10.1038/35088576, 11533719.
3. Rand DA, Shulgin BV, Salazar D, Millar AJ. Design principles underlying circadian clocks. J R Soc Interface 2004, 1:119-130. 10.1098/rsif.2004.0014, 1618932, 16849158.
4. Stelling J, Gilles ED, Doyle FJ. Robustness properties of circadian clock architectures. Proc Natl Acad Sci USA 2004, 101(36):13210-5. 10.1073/pnas.0401463101, 516549, 15340155.
5. Locke JCW, Southern MM, Kozma-Bognar L, Hibberd V, Brown PE, Turner MS, Millar AJ. Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 2005, 1:2005.0013. 10.1038/msb4100018, PMC1681447, 16729048, 16729048 .
6. Wagner A. Circuit topology and the evolution of robustness in two-gene circadian oscillators. Proc Natl Acad Sci USA 2005, 102(33):11775-80. 10.1073/pnas.0501094102, 1183445, 16087882.
7. Locke JCW, Kozma-Bognar L, Gould PD, Fehér B, Kevei E, Nagy F, Turner MS, Hall A, Millar AJ. Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol 2006, 2:59. 10.1038/msb4100102, PMC1682024, 17102804, 17102804.
8. Akman OE, Locke JCW, Tang S, Carré I, Millar AJ, Rand DA. Isoform switching facilitates period control in the Neurospora crassa circadian clock. Mol Syst Biol 2008, 4:64. PMC2267733, 18277380 .
9. Tsai TY, Choi Y, Ma W, Pomerening JR, Tang C, Ferrell JE. Robust, tunable biological oscillations from interlinked positive and negative feedback loops. Science 2009, 321(5885):126-9.
10. Kitano H. Biological robustness. Nat Rev Genet 2004, 5(11):826-37. 10.1038/nrg1471, 15520792.
11. Kitano H. Towards a theory of biological robustness. Mol Syst Biol 2007, 3:137. 10.1038/msb4100179, 2013924, 17882156.
12. Bell-Pedersen D, Crosthwaite SK, Lakin-Thomas PL, Merrow M, Okland M. The Neurospora circadian clock: simple or complex?. Philos Trans R Soc Lond B Biol Sci 2001, 356(1415):1697-1709. 10.1098/rstb.2001.0968, 1088545, 11710976.
13. Loros JJ, Dunlap JC. Genetic and molecular analysis of circadian rhythms in Neurospora. Annu Rev Physiol 2001, 63:757-794. 10.1146/annurev.physiol.63.1.757, 11181975.
14. Vitalini MW, de Paula RM, Park WD, Bell-Pedersen D. The rhythms of life: circadian output pathways in Neurospora. J Biol Rhythms 2006, 21(6):432-44. 10.1177/0748730406294396, 17107934.
15. Merrow M, Boesl C, Ricken J, Messerschmitt M, Goedel M, Roenneberg T. Entrainment of the Neurospora circadian clock. Chronobiol Int 2006, 23(1-2):71-80. 10.1080/07420520500545888, 16687281.
16. Tan Y, Dragovic Z, Roenneberg T, Merrow M. Entrainment dissociates transcription and translation of a circadian clock gene in Neurospora. Curr Biol 2004, 14(5):433-8. 10.1016/j.cub.2004.02.035, 15028220.
17. Merrow M, Brunner M, Roenneberg T. Assignment of circadian function for the Neurospora clock gene frequency. Nature 1999, 399:584-586. 10.1038/21190, 10376598.
18. Cheng P, Yang Y, Liu Y. Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock. Proc Natl Acad Sci USA 2001, 98(13):7408-13. 10.1073/pnas.121170298, 34682, 11416214.
19. Froehlich AC, Liu Y, Loros JJ, Dunlap JC. White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 2002, 297(5582):815-9. 10.1126/science.1073681, 12098706.
20. Garceau NY, Liu Y, Loros JJ, Dunlap JC. Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 1997, 89(3):469-76. 10.1016/S0092-8674(00)80227-5, 9150146.
21. Cheng P, Yang Y, Heintzen C, Liu Y. Coiled-coil domain-mediated FRQ-FRQ interaction is essential for its circadian clock function in Neurospora. EMBO J 2001, 20(1-2):101-8. 10.1093/emboj/20.1.101, 140186, 11226160.
22. Colot HV, Loros JJ, Dunlap JC. Temperature-modulated alternative splicing and promoter use in the circadian clock gene frequency. Mol Biol Cell 2005, 16(12):5563-5571. 10.1091/mbc.E05-08-0756, 1289402, 16195340.
23. Diernfellner AC, Schafmeier T, Merrow MW, Brunner M. Molecular mechanism of temperature sensing by the circadian clock of Neurospora crassa. Genes Dev 2005, 19(17):1968-73. 10.1101/gad.345905, 1199567, 16107616.
24. Denault DL, Loros JJ, Dunlap JC. WC-2 mediates WC1-FRQ interaction within the PAS protein-linked circadian feedback loop of Neurospora. EMBO J 2001, 20(1-2):109-17. 10.1093/emboj/20.1.109, 140181, 11226161.
25. Merrow M, Franchi L, Dragovic Z, Gorl M, Johnson J, Brunner M, Macino G, Roenneberg T. Circadian regulation of the light input pathway in Neurospora crassa. EMBO J 2001, 20(3):307-15. 10.1093/emboj/20.3.307, 133466, 11157738.
26. Froehlich AC, Loros JJ, Dunlap JC. Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc Natl Acad Sci USA 2003, 100(10):5914-9. 10.1073/pnas.1030057100, 156301, 12714686.
27. Schafmeier T, Haase A, Káldi K, Scholz J, Fuchs M, Brunner M. Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 2005, 122(2):235-46. 10.1016/j.cell.2005.05.032, 16051148.
28. Hong CI, Ruoff P, Loros JJ, Dunlap JC. Closing the circadian negative feedback loop: FRQ-dependent clearance of WC-1 from the nucleus. Genes Dev 2008, 22(22):3196-3204. 10.1101/gad.1706908, 2593610, 18997062.
29. Cheng P, He Q, Wang L, Liu Y. Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev 2005, 19(2):234-41. 10.1101/gad.1266805, 545885, 15625191.
30. Lee K, Loros JJ, Dunlap JC. Interconnected feedback loops in the Neurospora circadian system. Science 2000, 289(5476):107-10. 10.1126/science.289.5476.107, 10884222.
31. Crosthwaite SK, Loros JJ, Dunlap JC. Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 1995, 81(7):1003-12. 10.1016/S0092-8674(05)80005-4, 7600569.
32. Collett MA, Garceau N, Dunlap JC, Loros JJ. Light and clock expression of the Neurospora clock gene frequency is differentially driven by but dependent on WHITE-COLLAR-2. Genetics 2002, 160:149-58. 1461937, 11805052.
33. Leloup JC, Gonze D, Goldbeter A. Limit cycle models for circadian rhythms based on transcriptional regulation in Drosophila and Neurospora. J Biol Rhythms 1999, 14(6):433-448. 10.1177/074873099129000948, 10643740.
34. Smolen P, Baxter DA, Byrne JH. Modeling circadian oscillations with interlocking positive and negative feedback loops. J Neurosci 2001, 21(17):6644-56.
35. Gonze D, Halloy J, Goldbeter A. Robustness of circadian rhythms with respect to molecular noise. Proc Natl Acad Sci USA 2002, 99(2):673-8. 10.1073/pnas.022628299, 117364, 11792856.
36. Smolen P, Baxter DA, Byrne JH. Reduced models of the circadian oscillators in Neurospora crassa and Drosophila melanogaster illustrate mechanistic similarities. OMICS 2003, 7(4):337-54. 10.1089/153623103322637661, 14683608.
37. Francois P. A model for the Neurospora circadian clock. Biophys J 2005, 88(4):2369-2383. 10.1529/biophysj.104.053975, 1305337, 15653726.
38. Ruoff P, Loros JJ, Dunlap JC. The relationship between FRQ-protein stability and temperature compensation in the Neurospora circadian clock. Proc Natl Acad Sci USA 2005, 102(49):17681-6. 10.1073/pnas.0505137102, 1308891, 16314576.
39. Hong CI, Jolma IW, Loros JJ, Dunlap JC, Ruoff P. Simulating dark expressions and interactions of frq and wc-1 in the Neurospora circadian clock. Biophys J 2008, 94(4):1221-32. 10.1529/biophysj.107.115154, 2212688, 17965132.
40. Rand DA, Shulgin BV, Salazar JD, Millar AJ. Uncovering the design principles of circadian clocks: mathematical analysis of flexibility and evolutionary goals. J Theor Biol 2006, 238(3):616-635. 10.1016/j.jtbi.2005.06.026, 16111710.
41. Heintzen C, Loros JJ, Dunlap JC. The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 2001, 104(3):453-64. 10.1016/S0092-8674(01)00232-X, 11239402.
42. Shrode LB, Lewis ZA, White LD, Bell-Pedersen D, Ebbole DJ. vvd is required for light adaptation of conidiation-specific genes of Neurospora crassa, but not circadian conidiation. Fungal Genet Biol 2001, 32(3):169-181. 10.1006/fgbi.2001.1264, 11343403.
43. Schwerdtfeger C, Linden H. VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J 2003, 22(18):4846-4855. 10.1093/emboj/cdg451, 212719, 12970196.
44. Elvin M, Loros JJ, Dunlap JC, Heintzen HC. The PAS/LOV protein VIVID supports a rapidly dampened daytime oscillator that facilitates entrainment of the Neurospora circadian clock. Genes Dev 2005, 19(21):2593-605. 10.1101/gad.349305, 1276733, 16264193.
45. Brown KS, Sethna JP. Statistical mechanical approaches to models with many poorly known parameters. Phys Rev E 2003, 68:021904.
46. Locke JCW, Millar AJ, Turner MS. Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. J Theor Biol 2005, 234(3):383-93. 10.1016/j.jtbi.2004.11.038, 15784272.
47. Zeilinger MN, Farré EM, Taylor SR, Kay SA, Doyle FJ. A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol Syst Biol 2005, 2:58. PMC1682023, 17102803 .
48. Gutenkunst RN, Waterfall JJ, Casey FP, Brown K, Myers CR, Sethna JP. Universally sloppy parameter sensitivities in systems biology models. PLoS Comput Biol 2007, 3(10):1871-78. 10.1371/journal.pcbi.0030189, 2000971,2000971, 17922568.
49. Schafmeier T, Káldi K, Diernfellner A, Mohr C, Brunner M. Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toward a cytoplasmic activator. Cell 2006, 20(3):297-306.
50. Rand DA. Mapping global sensitivity of cellular network dynamics: sensitivity heat maps and a global summation Law. J R Soc Interface 2008, S59-69. 10.1098/rsif.2008.0084.focus, 2706458, 18482906.
51. Kurosawa G, Iwasa Y. Saturation of enzyme kinetics in circadian clock models. J Biol Rhythms 2002, 17(6):568-577. 10.1177/0748730402238239, 12465890.
52. DePaula RM, Vitalini MW, Gomer RH, Bell-Pedersen D. Complexity of the Neurospora crassa circadian clock system: multiple loops and oscillators. Cold Spring Harb Symp Quant Biol 2007, 72:345-51. 10.1101/sqb.2007.72.002, 18419292.
53. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH. Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 1998, 95(15):8660-4. 10.1073/pnas.95.15.8660, 21132, 9671734.
54. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AA. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 2005, 309:630-3. 10.1126/science.1115581, 16040710.
55. Bagheri N, Doyle FJ. Quantitative performance metrics for robustness in circadian rhythms. Bioinformatics 2007, 23(3):358-64. 10.1093/bioinformatics/btl627, 17158515.
56. Gunawan R, Doyle FJ. Phase sensitivity analysis of circadian rhythm entrainment. J Biol Rhythms 2007, 22(2):180-94. 10.1177/0748730407299194, 17440219.
57. Guckenheimer J, Holmes P. Nonlinear Oscillations, Dynamical Systems and Bifurcations of Vector Fields 1983, New York, Springer Verlag.
58. Dharmananda S. Studies of the circadian clock of Neurospora crassa: light-induced phase shifting. PhD thesis 1980, University of California, Santa Cruz.
59. Ueda HR, Hagiwara M, Kitano H. Robust oscillations within the interlocked feedback model of Drosophila circadian rhythm. J Theor Biol 2001, 210(4):401-6. 10.1006/jtbi.2000.2226, 11403560.
60. Gonze D, Halloy J, Goldbeter A. Biochemical clocks and molecular noise: theoretical study of robustness Factors. J Chem Phys 2002, 116:10997-11010.
61. Kurosawa G, Mochizuki A, Iwasa Y. Comparative study of circadian clock models, in search of processes promoting oscillation. J Theor Biol 2002, 216(2):193-208. 10.1006/jtbi.2002.2546, 12079371.
62. Leloup JC, Goldbeter A. Toward a detailed computational model for the mammalian circadian clock. Proc Natl Acad Sci USA 2003, 100(12):7051-6. 10.1073/pnas.1132112100, 165828, 12775757.
63. MacDonald N. Biological Delay Systems: Linear Stability Theory 1989, Cambridge, Cambridge University Press.
64. Sriram K, Gopinathan MS. A two variable delay model for the circadian rhythm of Neurospora crassa. J Theor Biol 2004, 231:23-38. 10.1016/j.jtbi.2004.04.006, 15363927.
65. Mittler JE, Sulzer B, Neumann A, Perelson AS. Influence of delayed viral production on viral dynamics in HIV-1 infected patients. Math Biosci 1998, 152(2):143-163. 10.1016/S0025-5564(98)10027-5, 9780612.