Delay-induced transient increase and heterogeneity in gene expression in negatively auto-regulated gene circuits

PLoS ONE

Volumn 3, Issue 8, 2008, Pages

  Maithreye, R ^a   Sarkar, Ram Rup ^a   Parnaik, Veena K ^a   Sinha, Somdatta ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTOREGULATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DYNAMICS; GENE CONTROL; GENE EXPRESSION; HOMEOSTASIS; NEGATIVE FEEDBACK; NONHUMAN; OSCILLATION; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; COMPUTER SIMULATION; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; KINETICS; SIGNAL TRANSDUCTION;

GREEN FLUORESCENT PROTEIN;

CIRCADIAN RHYTHM; COMPUTER SIMULATION; FEEDBACK, BIOCHEMICAL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GREEN FLUORESCENT PROTEINS; HOMEOSTASIS; KINETICS; MODELS, GENETIC; SIGNAL TRANSDUCTION;

EID: 51849124208     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002972     Document Type: Article

References (71)

1. Thieffry D, Huerta AM, Perez-Rueda E, Collado-Vides J (1998) From specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli. Bioessays 20: 433-440.
2. Shen-Orr S, Milo R, Mangan S, Alon U (2002) Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31: 64-69.
3. Milo R, Itzkovitz S, Kashtan N, Levitt R, Shen-Orr S, et al. (2004) Superfamilies of evolved and designed networks. Science 303: 1538-1542.
4. Alon U (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8: 450-461.
5. Kaern M, Elston TC, Blake WJ, Collins JJ (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6: 451-454.
6. Smolen P, Baxter DA, Byrne JH (2000) Mathematical modeling of gene networks. Neuron 26: 567-580.
7. Kepler TB, Elston TC (2001) Stochasticity in transcriptional regulation: origins, consequences and mathematical representations. Biophys J 81: 3116-3136.
8. Becskei A, Kaufmann BB, van Oudenaarden A (2005) Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat Genet 37: 937-944.
9. Colman-Lerner A, Gordon A, Serra E, Chin T, Resnekov O, et al. (2005) Regulated cell-to-cell variation in a cell-fate decision system. Nature 437: 699-706.
10. Hooshangi S, Weiss R (2006) The effect of negative feedback on noise propagation in transcriptional gene networks. Chaos 16: 026108.
11. Dublanche Y, Michalodimitrakis K, Kümmerer N, Foglierini M, Serrano L (2006) Noise in transcription negative feedback loops: simulation and experimental analysis. Mol Syst Biol 2: 41.
12. Maithreye R, Sinha S (2007) Propagation of extrinsic perturbation in a negatively auto-regulated pathway. Phys Biol 4: 48-59.
13. Levine E, Hwa T (2007) Stochastic fluctuations in metabolic pathways. Proc Natl Acad Sci USA 104: 9224-9229.
14. Ptashne M (2004) A Genetic Switch: Phage Lambda Revisited. 3rd Ed. Cold Spring Harbor, New York: CSHL Press. 154 p.
15. Gardner TS, Cantor CR, Collins JJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339-342.
16. Tyson JJ (1991) Modeling cell division cycle: cdc2 and cyclin interactions. Proc Natl Acad Sci USA 88: 7328-7332.
17. Bar-Or RL, Maya R, Segel LA, Alon U, Levine AJ, et al. (2000) Generation of oscillations by the p53-Mdm2 feedback loop: a theoretical and experimental study. Proc Natl Acad Sci USA 97: 11250-11255.
18. Roenneberg T, Merrow M (2003) The network, of time: understanding the molecular circadian system. Curr Biol 13: R198-R207.
19. Becskei A, Seraphin B, Serrano L (2001) Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion. EMBO J 20: 2528-2535.
20. Ozbudak EM, Thattai M, Lim HN, Shraiman BI, van Oudenaarden A (2004) Multistability in the lactose utilization network of Escherichia coli. Nature 427: 737-740.
21. Maeda YT, Sano M (2006) Regulatory dynamics of synthetic gene networks with positive feedback. J Mol Biol 359: 1107-1124.
22. Van Hoek MJA, Hogeweg P (2006) In silico evolved lac operons exhibit bistability for artificial inducers but not for lactose. Biophys J 91: 2833-2843.
23. Maamar H, Raj A, Dubnau D (2007) Noise in gene expression determines cell fate in Bacillus subtilis. Science 317: 526-529.
24. Sureka K, Ghosh B, Dasgupta A, Basu J, Kundu M, et al. (2008) Positive feedback and noise activate the stringent response regulator Rel in Mycobacteria. PLoS ONE 3(3): e1771 doi:10.1371/journal.pone.0001771.
25. Goodwin BC (1965) Oscillatory behavior of enzymatic control processes. Adv Enzyme Regul 3: 425-439.
26. Sinha S, Ramaswamy R (1988) Complex behaviour of the repressible operon. J Theor Biol 132: 307-318.
27. Becskei A, Serrano L (2000) Engineering stability in gene networks by autoregulation Nature 405: 590-593.
28. Elowitz MB, Leibler S (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403: 335-338.
29. Rosenfeld N, Elowitz MB, Alon U (2002) Negative autoregulation speeds the response times of transcription networks. J Mol Biol 323: 785-793.
30. Mangan S, Zaslayer A, Alon U (2003) The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J Mol Biol 334: 197-204.
31. Monk N (2003) Oscillatory expression of Hesl, p53, and NF-κB driven by transcriptional time delays. Curr Biol 13: 1409-1413.
32. Tiana G, Krishna S, Pigolotti S, Jensen MH, Sneppen K (2007) Oscillations and temporal signalling in cells. Phys Biol 4: R1-R17.
33. Weinberger LS, Shenk T (2007) An HIV feedback resistor: Auto-regulatory circuit deactivator and noise buffer. PLoS Biol 5: e9 doi:10.1371/ journal.pbio.0050009.
34. Savageau MA (1974) Comparison of classical and autogenous systems of regulation in inducible operons. Nature 252: 546-549.
35. Rao CV, Wolf DM, Arkin AP (2002) Control, exploitation and tolerance of intracellular noise. Nat Genet 420: 231-237.
36. McAdams HH, Arkin A (1997) Stochastic mechanisms in gene expression. Proc Natl Acad Sci USA 94: 814-819.
37. Austin DW, Allen MS, McCollum JM, Dar RD, Wilgus JR, et al. (2006) Gene network shaping of inherent noise spectra. Nature 439: 608-611.
38. Simpson ML, Cox CD, Sayler GS (2003) Frequency domain analysis of noise in autoregulated gene circuits. Proc Natl Acad Sci USA 100: 4551-4556.
39. Struhl K (1999) Fundamentally different logic of gene regulation in eukaryotes and prokaryotes Cell 98: 1-4.
40. Rosenfeld N, Alon U (2003) Response delays and the structure of transcription networks. J Mol Biol 329: 645-654.
41. Rapp PE (1975) A theoretical investigation of a large class of biochemical oscillators. Math Biosc 25: 165-188.
42. Maithreye R, Sinha S (2003) Modelling of simple biochemical pathways. In: Deutsch A, Falcke M, Howard J, Zimmermann W, eds. Function and regulation of cellular systems: Experiments and Models. Birkhauser. pp 251-257.
43. Gopalsamy, K (1992) Stability and oscillations in delay differential equations of population dynamics. Springer. 520 p.
44. Bratsun D, Volfson D, Tsimring LS, Hasty J (2005) Delay-induced stochastic oscillations in gene regulation. Proc Natl Acad Sci USA 102: 14593-14598.
45. Ozbudak EM, Thattai M, Kurtser I, Grossman AD, van Oudenaarden A (2002) Regulation of noise in the expression of a single gene. Nat Genet 31: 69-73.
46. Swain PS, Elowitz MB, Siggia ED (2002) Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc Natl Acad Sci USA 99: 12795-12800.
47. Blake WJ, Kaern M, Cantor GR, Collins JJ (2003) Noise in eukaryotic gene expression, Nature 422: 633-637.
48. Raser JM, O'Shea EK (2004) Control of stochasticity in eukaryotic gene expression. Science 304: 1811-1814.
49. Chen L, Wang R, Zhou T, Aihara K (2005) Noise-induced cooperative behavior in a multicell system. Bioinformatics 21: 2722-2729.
50. Hooshangi S, Thiberge S, Weiss R (2005) Ultrasensitivity and noise propagation in a synthetic transcriptional cascade. Proc Natl Acad Sci U S A 102: 3581-3586.
51. Pedraza JM, van Oudenaarden A (2005) Noise propagation in gene networks. Science 307: 1965-1969.
52. Banerjee B, Balasubramanian S, Ananthakrishna G, Ramakrishnan TV, Shivashankar GV (2004) Tracking operator state fluctuations in gene expression in single cells. Biophys J 86: 3052-3059.
53. Basu S, Mehreja R, Thiberge S, Chen MT, Weiss R (2004) Spatiotemporal control of gene expression with pulse-generating networks. Proc Natl Acad Sci U S A 101: 6355-6360.
54. Freedman HI, Gopalsamy K (1986) Global stability in time-delayed single species dynamics. Bull Math Biol 48: 485-492.
55. Niculescu S (1998) Stability and hyperbolicity of linear systems with delayed state: a matrix-pencil approach. IMA J of Math Control & Information. 15: 331-347.
56. McAdams HH, Arkin A (1999) It's a noisy business! Genetic regulation at the nanomolar scale. Trends Genet 15: 65-69.
57. Losick R, Desplan C (2008) Stochasticity and cell fate. Science 320: 65-68.
58. Thieffry D, Thomas R (1995) Dynamical behaviour of biological regulatory networks - II. Immunity control in bacteriophage lambda. Bull Math Biol 57: 277-297.
59. Nelson DL, Cox MM (2007) Lehninger Principles of Biochemistry. New York: WH Freeman and Company. 1100 p.
60. Alpers D, Tomkins G (1966) Sequential transcription of the genes of the lactose operon and its regulation by protein synthesis. J Biol Chem 241: 4434-4443.
61. Goldberger R, Berberich M (1965) Sequential repression and derepression of enzymes for his biosynthesis in Salmonella typhimurium. Proc Nat Acad Sci USA 54: 279-286.
62. Starlinger P (1967) Sequential appearance of galactose enzymes in Escherichia coli. Mol Gen Genet 100: 10-215.
63. Zaslaver A, Mayo AE, Rosenberg R, Bashkin P, Sberro H, et al. (2004) Just-in-time transcription program in metabolic pathways. Nat Genet 36: 486-491.
64. Le TT, Emonet T, Harlepp S, Guet CC, Cluzel P (2006) Dynamical determinants of inducible gene expression in a single bacterium. Biophys J 90: 3315-3321.
65. Paulsson J (2004) Summing up the noise in gene networks. Nature 427: 415-418.
66. Shin D, Lee EJ, Huang H, Groisman EA (2006) A positive feedback loop promotes transcription surge that jump-starts Salmonella virulence circuit. Science 314: 1607-1609.
67. Suel GM, Garcia-Ojalvo J, Liberman LM, Elowitz MB (2006) An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440: 545-550.
68. Raser JM, O'Shea EK (2005) Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013.
69. Andersen JB, Sternberg C, Poulsen LK, Bjørn SP, Givskov M, et al. (1998) New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 64: 2240-2246.
70. Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81: 2340-2361.
71. Segel L (1980) Mathematical models in molecular and cellular biology. Cambridge: Cambridge University Press. 786 p.