DNA-Binding Kinetics Determines the Mechanism of Noise-Induced Switching in Gene Networks

Biophysical Journal

Volumn 109, Issue 8, 2015, Pages 1746-1757

  Tse, Margaret J ^a   Chu, Brian K ^a   Roy, Mahua ^a   Read, Elizabeth L ^a,b  

^a University of California at Irvine   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ALGORITHM; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENE EXPRESSION REGULATION; KINETICS; METABOLISM; PHYSIOLOGY; VALIDATION STUDY;

ALGORITHMS; COMPUTER SIMULATION; DNA; GENE EXPRESSION REGULATION; KINETICS; MODELS, BIOLOGICAL;

EID: 84944769246     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.08.035     Document Type: Article

References (74)

1. S. Kauffman Control circuits for determination and transdetermination Science 181 1973 310 318
2. S. Huang, and G. Eichler D. Ingber Cell fates as high-dimensional attractor states of a complex gene regulatory network Phys. Rev. Lett. 94 2005 128701
3. S. Huang Reprogramming cell fates: reconciling rarity with robustness BioEssays 31 2009 546 560
4. B. Zhang, and P. Wolynes Stem cell differentiation as a many-body problem Proc. Natl. Acad. Sci. USA 111 2014 10185 10190
5. J. Wang, and K. Zhang E. Wang Quantifying the Waddington landscape and biological paths for development and differentiation Proc. Natl. Acad. Sci. USA 108 2011 8257 8262
6. T. Hong, and J. Xing J. Tyson A mathematical model for the reciprocal differentiation of T helper 17 cells and induced regulatory T cells PLOS Comput. Biol. 7 2011 e1002122
7. S. Huang, and S. Kauffman How to escape the cancer attractor: Rationale and limitations of multi-target drugs Semin. Cancer Biol. 23 2013 270 278
8. D.A. Beard, and H. Qian Chemical Biophysics: Quantitative Analysis of Cellular Systems 2008 Cambridge University Press Cambridge, United Kingdom
9. A. Raj, and A. van Oudenaarden Nature, nurture, or chance: stochastic gene expression and its consequences Cell 135 2008 216 226
10. K. Miller-Jensen, and S. Dey A. Arkin Varying virulence: epigenetic control of expression noise and disease processes Trends Biotechnol. 29 2011 517 525
11. A. Arkin, J. Ross, and H. McAdams Stochastic kinetic analysis of developmental pathway bifurcation in phage lambda-infected Escherichia coli cells Genetics 149 1997 1633 1648
12. L.S. Weinberger, and J.C. Burnett D.V. Schaffer Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity Cell 122 2005 169 182
13. D.A. Hume Probability in transcriptional regulation and its implications for leukocyte differentiation and inducible gene expression Blood 96 2000 2323 2328
14. P.J. Choi, and L. Cai X.S. Xie A stochastic single-molecule event triggers phenotype switching of a bacterial cell Science 322 2008 442 446
15. H.H. Chang, and M. Hemberg S. Huang Transcriptome-wide noise controls lineage choice in mammalian progenitor cells Nature 453 2008 544 547
16. J.-E. Dietrich, and T. Hiiragi Stochastic patterning in the mouse pre-implantation embryo Development 134 2007 4219 4231
17. N. Balaban, and J. Merrin S. Leibler Bacterial persistence as a phenotypic switch Science 305 2004 1622 1625
18. M. Acar, J.T. Mettetal, and A. van Oudenaarden Stochastic switching as a survival strategy in fluctuating environments Nat. Genet. 40 2008 471 475
19. S. Sharma, and D. Lee J. Settleman A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations Cell 141 2010 69 80
20. D. Gillespie Exact stochastic simulation of coupled chemical reactions J. Phys. Chem. 81 1977 2340 2361
21. T. Kepler, and T. Elston Stochasticity in transcriptional regulation: origins, consequences, and mathematical representations Biophys. J. 81 2000 3116 3136
22. J. Hasty, and J. Pradines J. Collins Noise-based switches and amplifiers for gene expression Proc. Natl. Acad. Sci. USA 97 2000 2075 2080
23. T. Gardner, C. Cantor, and J. Collins Construction of a genetic toggle switch in Escherichia coli Nature 403 2000 339 342
24. E. Segal, and J. Widom From DNA sequence to transcriptional behaviour: a quantitative approach Nat. Rev. Genet. 10 2009 443 456
25. M. Sasai, and P.G. Wolynes Stochastic gene expression as a many-body problem Proc. Natl. Acad. Sci. USA 100 2003 2374 2379
26. M. Sasai, and Y. Kawabata T. Terada Time scales in epigenetic dynamics and phenotypic heterogeneity of embryonic stem cells PLOS Comput. Biol. 9 2013 e1003380
27. C. Li, and J. Wang Quantifying Waddington landscapes and paths of non-adiabatic cell fate decisions for differentiation, reprogramming and transdifferentiation J. R. Soc. Interface 10 2013 20130787
28. H. Feng, B. Han, and J. Wang Landscape and global stability of nonadiabatic and adiabatic oscillations in a gene network Biophys. J. 102 2012 1001 1010
29. H. Ge, H. Qian, and X.S. Xie Stochastic phenotype transition of a single cell in an intermediate region of gene state switching Phys. Rev. Lett. 114 2015 078101
30. A.M. Walczak, J.N. Onuchic, and P.G. Wolynes Absolute rate theories of epigenetic stability Proc. Natl. Acad. Sci. USA 102 2005 18926 18931
31. H. Feng, and J. Wang A new mechanism of stem cell differentiation through slow binding/unbinding of regulators to genes Sci. Rep. 2 2012 550
32. M. Lu, J. Onuchic, and E. Ben-Jacob Construction of an effective landscape for multistate genetic switches Phys. Rev. Lett. 113 2014 078102
33. D.M. Roma, and R.A. O'Flanagan R. Mukhopadhyay Optimal path to epigenetic switching Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71 2005 011902
34. E. Aurell, and K. Sneppen Epigenetics as a first exit problem Phys. Rev. Lett. 88 2002 048101
35. J. Zhou, and M. Aliyu S. Huang Quasi-potential landscape in complex multi-stable systems J. R. Soc. Interface 9 2012 3539 3553
36. P. Wang, and C. Song J. Xing Epigenetic state network approach for describing cell phenotypic transitions Interface Focus 4 2014 20130068
37. K. Zhang, M. Sasai, and J. Wang Eddy current and coupled landscapes for nonadiabatic and nonequilibrium complex system dynamics Proc. Natl. Acad. Sci. USA 110 2013 14930 14935
38. M. Morelli, and S. Tanase-Nicola P. ten Wolde Reaction coordinates for the flipping of genetic switches Biophys. J. 94 2008 3413 3423
39. M. Strasser, F.J. Theis, and C. Marr Stability and multiattractor dynamics of a toggle switch based on a two-stage model of stochastic gene expression Biophys. J. 102 2012 19 29
40. D. Schultz, and A.M. Walczak P.G. Wolynes Extinction and resurrection in gene networks Proc. Natl. Acad. Sci. USA 105 2008 19165 19170
41. A. Lipshtat, and A. Loinger O. Biham Genetic toggle switch without cooperative binding Phys. Rev. Lett. 96 2006 188101
42. R. Ma, and J. Wang H. Liu Small-number effects: a third stable state in a genetic bistable toggle switch Phys. Rev. Lett. 109 2012 248107
43. M.N. Artyomov, and M. Mathur A.K. Chakraborty Stochastic bimodalities in deterministically monostable reversible chemical networks due to network topology reduction J. Chem. Phys. 131 2009 195103
44. R. Allen, C. Valeriani, and P. ten Wolde Forward flux sampling for rare event simulations J. Phys. Condens. Matter 21 2009 463102
45. A. Dickson, A. Warmflash, and A.R. Dinner Nonequilibrium umbrella sampling in spaces of many order parameters J. Chem. Phys. 130 2009 074104
46. R. Donovan, and A. Sedgewick D. Zuckerman Efficient stochastic simulation of chemical kinetics networks using a weighted ensemble of trajectories J. Chem. Phys. 139 2013 115105
47. C. Schütte, and F. Noé E. Vanden-Eijnden Markov state models based on milestoning J. Chem. Phys. 134 2011 204105
48. A. Dickson, A. Warmflash, and A.R. Dinner Separating forward and backward pathways in nonequilibrium umbrella sampling J. Chem. Phys. 131 2009 154104
49. E. Vanden-Eijnden, and M. Venturoli Revisiting the finite temperature string method for the calculation of reaction tubes and free energies J. Chem. Phys. 130 2009 194103
50. J. Adelman, and M. Grabe Simulating rare events using a weighted ensemble-based string method J. Chem. Phys. 138 2013 044105
51. M. Ptashne A Genetic Switch 3rd ed. 2004 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
52. H. Niwa, and Y. Toyooka J. Rossant Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation Cell 123 2005 917 929
53. P. Zhang, and G. Behre Z. Sun Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1 Proc. Natl. Acad. Sci. USA 96 1999 8705 8710
54. T. Hong, and J. Xing J. Tyson A simple theoretical framework for understanding heterogeneous differentiation of CD4+ T cells BMC Syst. Biol. 6 2012 66
55. C. Waddington, and H. Kacser The Strategy of the Genes 1957 Routledge London
56. S. Huang The molecular and mathematical basis of Waddington's epigenetic landscape: a framework for post-Darwinian biology? BioEssays 34 2012 149 157
57. G. Huber, and S. Kim Weighted-ensemble Brownian dynamics simulations for protein association reactions Biophys. J. 70 1996 97 110
58. E.W.W. Ren, and E. Vanden-Eijnden Transition pathways in complex systems: reaction coordinates, isocommittor surfaces, and transition tubes Chem. Phys. Lett. 413 2005 242 247
59. M.C. Zwier, and L.T. Chong Reaching biological timescales with all-atom molecular dynamics simulations Curr. Opin. Pharmacol. 10 2010 745 752
60. R.J. Allen, P.B. Warren, and P.R. ten Wolde Sampling rare switching events in biochemical networks Phys. Rev. Lett. 94 2005 018104
61. A. Dickson, and A.R. Dinner Enhanced sampling of nonequilibrium steady states Annu. Rev. Phys. Chem. 61 2010 441 459
62. N.G. Van Kampen Stochastic Processes in Physics and Chemistry 3rd ed. 2007 Elsevier Amsterdam
63. MATLAB and Parallel Computing Toolbox Release. 2012b. The MathWorks, Natick, MA.
64. J.R. Faeder, M.L. Blinov, and W.S. Hlavacek Rule-based modeling of biochemical systems with BioNetGen Methods Mol. Biol. 500 2009 113 167
65. M.C. Zwier, and J.L. Adelman L.T. Chong WESTPA: An interoperable, highly scalable software package for weighted ensemble simulation and analysis J. Chem. Theory Comput. 11 2015 800 809
66. A. Ma, and A.R. Dinner Automatic method for identifying reaction coordinates in complex systems J. Phys. Chem. B 109 2005 6769 6779
67. Y. Yamanaka, F. Lanner, and J. Rossant FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst Development 137 2010 715 724
68. A.M. Singh, and T. Hamazaki N. Terada A heterogeneous expression pattern for Nanog in embryonic stem cells Stem Cells 25 2007 2534 2542
69. I. Chambers, and J. Silva A. Smith Nanog safeguards pluripotency and mediates germline development Nature 450 2007 1230 1234
70. T. Kalmar, and C. Lim A. Martinez Arias Regulated fluctuations in Nanog expression mediate cell fate decisions in embryonic stem cells PLoS Biol. 7 2009 e1000149
71. Y. Buganim, and D.A. Faddah R. Jaenisch Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase Cell 150 2012 1209 1222
72. L. Mariani, and E. Schulz T. Höfer Short-term memory in gene induction reveals the regulatory principle behind stochastic IL-4 expression Mol. Syst. Biol. 6 2010 359
73. E.E. Borrero, and F.A. Escobedo Reaction coordinates and transition pathways of rare events via forward flux sampling J. Chem. Phys. 127 2007 164101
74. E.W.W. Ren, and E. Vanden-Eijnden String method for the study of rare events Phys. Rev. B 66 2002 052301