A minimal transcriptional controlling network of regulatory T cell development

Journal of Physical Chemistry B

Volumn 117, Issue 42, 2013, Pages 12995-13004

  Liao, Chen ^a   Lu, Ting ^a  

^a University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CYTOLOGY; DYNAMICS; T-CELLS;

COMPLEX REGULATORY NETWORK; DNA BINDING AFFINITY; DYNAMIC FEATURES; ENVIRONMENTAL FLUCTUATIONS; MULTI STABILITIES; NEGATIVE FEEDBACK LOOP; PARAMETER REGIMES; REGULATORY T CELLS;

FEEDBACK;

DNA; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

ARTICLE; CHEMICAL STRUCTURE; GENE REGULATORY NETWORK; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MUTATION; PROTEIN BINDING; REGULATORY T LYMPHOCYTE;

DNA; FORKHEAD TRANSCRIPTION FACTORS; GENE REGULATORY NETWORKS; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; T-LYMPHOCYTES, REGULATORY;

EID: 84886712702     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp402306g     Document Type: Article

References (86)

1. Belkaid, Y.; Rouse, B. T. Natural Regulatory T Cells in Infectious Disease Nat. Immunol. 2005, 6, 353-360
2. Sakaguchi, S.; Yamaguchi, T.; Nomura, T.; Ono, M. Regulatory T Cells and Immune Tolerance Cell 2008, 133, 775-787
3. Miyara, M.; Sakaguchi, S. Natural Regulatory T Cells: Mechanisms of Suppression Trends Mol. Med. 2007, 13, 108-116
4. Josefowicz, S. Z.; Lu, L.-F.; Rudensky, A. Y. Regulatory T Cells: Mechanisms of Differentiation and Function Annu. Rev. Immunol. 2012, 30, 531-564
5. Fontenot, J. D.; Rudensky, A. Y. A Well Adapted Regulatory Contrivance: Regulatory T Cell Development and the Forkhead Family Transcription Factor Foxp3 Nat. Immunol. 2005, 6, 331-337
6. Ramsdell, F. Foxp3 and Natural Regulatory T Cells: Key to a Cell Lineage? Immunity 2003, 19, 165-168
7. Zheng, Y.; Rudensky, A. Y. Foxp3 in Control of the Regulatory T Cell Lineage Nat. Immunol. 2007, 8, 457-462
8. Hori, S.; Nomura, T.; Sakaguchi, S. Control of Regulatory T Cell Development by the Transcription Factor Foxp3 Sci. Signaling 2003, 299, 1057-1061
9. Fontenot, J. D.; Gavin, M. A.; Rudensky, A. Y. Foxp3 Programs the Development and Function of CD4+CD25+ Regulatory T Cells Nat. Immunol. 2003, 4, 330-336
10. Khattri, R.; Cox, T.; Yasayko, S.-A.; Ramsdell, F. An Essential Role for Scurfin in CD4+CD25+ T Regulatory Cells Nat. Immunol. 2003, 4, 337-342
11. Williams, L. M.; Rudensky, A. Y. Maintenance of the Foxp3-Dependent Developmental Program in Mature Regulatory T Cells Requires Continued Expression of Foxp3 Nat. Immunol 2007, 8, 277-284
12. Zheng, Y.; Josefowicz, S. Z.; Kas, A.; Chu, T.-T.; Gavin, M. A.; Rudensky, A. Y. Genome-Wide Analysis of Foxp3 Target Genes in Developing and Mature Regulatory T Cells Nature (London) 2007, 445, 936-940
13. Marson, A.; Kretschmer, K.; Frampton, G. M.; Jacobsen, E. S.; Polansky, J. K.; MacIsaac, K. D.; Levine, S. S.; Fraenkel, E.; Von Boehmer, H.; Young, R. A. Foxp3 Occupancy and Regulation of Key Target Genes During T-Cell Stimulation Nature (London) 2007, 445, 931-935
14. Gavin, M. A.; Rasmussen, J. P.; Fontenot, J. D.; Vasta, V.; Manganiello, V. C.; Beavo, J. A.; Rudensky, A. Y. Foxp3-Dependent Programme of Regulatory T-Cell Differentiation Nature (London) 2007, 445, 771-775
15. Lin, W.; Haribhai, D.; Relland, L. M.; Truong, N.; Carlson, M. R.; Williams, C. B.; Chatila, T. A. Regulatory T Cell Development in the Absence of Functional Foxp3 Nat. Immunol. 2007, 8, 359-368
16. Pfoertner, S.; Jeron, A.; Probst-Kepper, M.; Guzman, C. A.; Hansen, W.; Westendorf, A. M.; Toepfer, T.; Schrader, A. J.; Franzke, A.; Buer, J. Signatures of Human Regulatory T Cells: An Encounter with Old Friends and New Players Genome Biol. 2006, 7, R54
17. Birzele, F.; Fauti, T.; Stahl, H.; Lenter, M. C.; Simon, E.; Knebel, D.; Weith, A.; Hildebrandt, T.; Mennerich, D. Next-Generation Insights into Regulatory T Cells: Expression Profiling and FoxP3 Occupancy in Human Nucleic Acids Res. 2011, 39, 7946-7960
18. Hill, J. A.; Feuerer, M.; Tash, K.; Haxhinasto, S.; Perez, J.; Melamed, R.; Mathis, D.; Benoist, C. Foxp3 Transcription-Factor-Dependent and -Independent Regulation of the Regulatory T Cell Transcriptional Signature Immunity 2007, 27, 786-800
19. Delgoffe, G. M.; Bettini, M. L.; Vignali, D. A. Identity Crisis: It's Not Just Foxp3 Anymore Immunity 2012, 37, 759-761
20. Rudra, D.; Chaudhry, A.; Niec, R. E.; Arvey, A.; Samstein, R. M.; Leslie, C.; Shaffer, S. A.; Goodlett, D. R.; Rudensky, A. Y. Transcription Factor Foxp3 and Its Protein Partners Form a Complex Regulatory Network Nat. Immunol. 2012, 13, 1010-1019
21. Fu, W.; Ergun, A.; Lu, T.; Hill, J. A.; Haxhinasto, S.; Fassett, M. S.; Gazit, R.; Adoro, S.; Glimcher, L.; Chan, S. A Multiply Redundant Genetic Switch 'Locks in' the Transcriptional Signature of Regulatory T Cells Nat. Immunol. 2012, 13, 972-980
22. Hori, S. The Foxp3 Interactome: A Network Perspective of Treg Cells Nat. Immunol. 2012, 13, 943-945
23. Rubtsov, Y. P.; Niec, R. E.; Josefowicz, S.; Li, L.; Darce, J.; Mathis, D.; Benoist, C.; Rudensky, A. Y. Stability of the Regulatory T Cell Lineage in Vivo Science 2010, 329, 1667-1671
24. Bailey-Bucktrout, S. L.; Bluestone, J. A. Regulatory T Cells: Stability Revisited Trends Immunol. 2011, 32, 301-306
25. Hamann, A. Regulatory T Cells Stay on Course Immunity 2012, 36, 161-163
26. Miyao, T.; Floess, S.; Setoguchi, R.; Luche, H.; Fehling, H. J.; Waldmann, H.; Huehn, J.; Hori, S. Plasticity of Foxp3 T Cells Reflects Promiscuous Foxp3 Expression in Conventional T Cells but Not Reprogramming of Regulatory T Cells Immunity 2012, 36, 262-275
27. Mendoza, L.; Pardo, F. A Robust Model to Describe the Differentiation of T-Helper Cells Theory Biosci. 2010, 129, 283-293
28. Hong, T.; Xing, J.; Li, L.; Tyson, J. J. A Mathematical Model for the Reciprocal Differentiation of T Helper 17 Cells and Induced Regulatory T Cells PLoS Comput. Biol. 2011, 7, e1002122
29. Hong, T.; Xing, J.; Li, L.; Tyson, J. A Simple Theoretical Framework for Understanding Heterogeneous Differentiation of CD4+ T Cells BMC Syst. Biol. 2012, 6, 66
30. Roeder, I.; Glauche, I. Towards an Understanding of Lineage Specification in Hematopoietic Stem Cells: A Mathematical Model for the Interaction of Transcription Factors GATA-1 and PU.1 J. Theory Biol. 2006, 241, 852-865
31. Kitano, H. Biological Robustness Nat. Rev. Genet. 2004, 5, 826-837
32. Stelling, J.; Sauer, U.; Szallasi, Z.; Doyle, F. J.; Doyle, J. Robustness of Cellular Functions Cell 2004, 118, 675-685
33. Barkai, N.; Shilo, B.-Z. Variability and Robustness in Biomolecular Systems Mol. Cell 2007, 28, 755-760
34. Li, F.; Long, T.; Lu, Y.; Ouyang, Q.; Tang, C. The Yeast Cell-Cycle Network is Robustly Designed Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 4781-4786
35. Little, J. W.; Shepley, D. P.; Wert, D. W. Robustness of a Gene Regulatory Circuit EMBO J. 1999, 18, 4299-4307
36. Shah, N. A.; Sarkar, C. A. Robust Network Topologies for Generating Switch-Like Cellular Responses PLoS Comput. Biol. 2011, 7, e1002085
37. Venturelli, O. S.; El-Samad, H.; Murray, R. M. Synergistic Dual Positive Feedback Loops Established by Molecular Sequestration Generate Robust Bimodal Response Proc. Natl. Acad. Sci. U.S.A. 2012, 109, E3324-E3333
38. Kærn, M.; Elston, T. C.; Blake, W. J.; Collins, J. J. Stochasticity in Gene Expression: From Theories to Phenotypes Nat. Rev. Genet. 2005, 6, 451-464
39. Raj, A.; van Oudenaarden, A. Nature, Nurture, or Chance: Stochastic Gene Expression and Its Consequences Cell 2008, 135, 216-226
40. Balázsi, G.; van Oudenaarden, A.; Collins, J. J. Cellular Decision Making and Biological Noise: From Microbes to Mammals Cell 2011, 144, 910-925
41. Swain, P. S.; Elowitz, M. B.; Siggia, E. D. Intrinsic and Extrinsic Contributions to Stochasticity in Gene Expression Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12795-12800
42. Lu, T.; Ferry, M.; Weiss, R.; Hasty, J. A Molecular Noise Generator Phys. Biol. 2008, 5, 036006
43. Rao, C. V.; Wolf, D. M.; Arkin, A. P. Control, Exploitation and Tolerance of Intracellular Noise Nature (London) 2002, 420, 231-237
44. Zhuravlev, P. I.; Papoian, G. A. Molecular Noise of Capping Protein Binding Induces Macroscopic Instability in Filopodial Dynamics Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 11570-11575
45. Raser, J. M.; O'Shea, E. K. Noise in Gene Expression: Origins, Consequences, and Control Science 2005, 309, 2010-2013
46. Sasai, M.; Wolynes, P. G. Stochastic Gene Expression as a Many-Body Problem Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 2374-2379
47. Aurell, E.; Sneppen, K. Epigenetics as a First Exit Problem Phys. Rev. Lett. 2002, 88, 48101
48. Wang, J.; Zhang, K.; Wang, E. Kinetic Paths, Time Scale, and Underlying Landscapes: A Path Integral Framework to Study Global Natures of Nonequilibrium Systems and Networks J. Chem. Phys. 2010, 133, 125103
49. Assaf, M.; Roberts, E.; Luthey-Schulten, Z. Determining the Stability of Genetic Switches: Explicitly Accounting for mRNA Noise Phys. Rev. Lett. 2011, 106, 248102
50. Zong, C.; Lu, T.; Shen, T.; Wolynes, P. G. Nonequilibrium Self-Assembly of Linear Fibers: Microscopic Treatment of Growth, Decay, Catastrophe and Rescue Phys. Biol. 2006, 3, 83-92
51. Tian, T.; Burrage, K. Stochastic Models for Regulatory Networks of the Genetic Toggle Switch Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 8372-8377
52. Shen, T.; Hamelberg, D. A Statistical Analysis of the Precision of Reweighting-Based Simulations J. Chem. Phys. 2008, 129, 034103
53. Lu, T.; Volfson, D.; Tsimring, L.; Hasty, J. Cellular Growth and Division in the Gillespie Algorithm Syst. Biol. 2004, 1, 121-128
54. Gillespie, D. T. Exact Stochastic Simulation of Coupled Chemical Reactions J. Phys. Chem. 1977, 81, 2340-2361
55. Dhooge, A.; Govaerts, W.; Kuznetsov, Y. A. MATCONT: A MATLAB Package for Numerical Bifurcation Analysis of ODEs ACM Trans. Math. Software 2003, 29, 141-164
56. Gillespie, D. T. Stochastic Simulation of Chemical Kinetics Annu. Rev. Phys. Chem. 2007, 58, 35-55
57. Süel, G. M.; Garcia-Ojalvo, J.; Liberman, L. M.; Elowitz, M. B. An Excitable Gene Regulatory Circuit Induces Transient Cellular Differentiation Nature (London) 2006, 440, 545-550
58. Milo, R.; Jorgensen, P.; Moran, U.; Weber, G.; Springer, M. BioNumbers-The Database of Key Numbers in Molecular and Cell Biology Nucleic Acids Res. 2010, 38, D750-D753
59. Wales, D. Energy Landscapes: Applications to Clusters, Biomolecules and Glasses; Cambridge University Press: Cambridge, U.K., 2004.
60. Zheng, W.; Schafer, N. P.; Davtyan, A.; Papoian, G. A.; Wolynes, P. G. Predictive Energy Landscapes for Protein-Protein Association Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 19244-19249
61. Onuchic, J. N.; Luthey-Schulten, Z.; Wolynes, P. G. Theory of Protein Folding: The Energy Landscape Perspective Annu. Rev. Phys. Chem. 1997, 48, 545-600
62. Lapidus, S.; Han, B.; Wang, J. Intrinsic Noise, Dissipation Cost, and Robustness of Cellular Networks: The Underlying Energy Landscape of MAPK Signal Transduction Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 6039-6044
63. Wang, J.; Xu, L.; Wang, E.; Huang, S. The Potential Landscape of Genetic Circuits Imposes the Arrow of Time in Stem Cell Differentiation Biophys. J. 2010, 99, 29-39
64. Wang, J.; Li, C.; Wang, E. Potential and Flux Landscapes Quantify the Stability and Robustness of Budding Yeast Cell Cycle Network Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 8195-8200
65. Wang, J.; Zhang, K.; Xu, L.; Wang, E. Quantifying the Waddington Landscape and Biological Paths for Development and Differentiation Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 8257-8262
66. Zhang, F.; Xu, L.; Zhang, K.; Wang, E.; Wang, J. The Potential and Flux Landscape Theory of Evolution J. Chem. Phys. 2012, 137, 065102
67. Cao, Y.; Lu, H.-M.; Liang, J. Probability Landscape of Heritable and Robust Epigenetic State of Lysogeny in Phage Lambda Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 18445-18450
68. Strasser, M.; Theis, F. J.; Marr, C. Stability and Multiattractor Dynamics of a Toggle Switch Based on a Two-Stage Model of Stochastic Gene Expression Biophys. J. 2012, 102, 19-29
69. Kim, K.-Y.; Wang, J. Potential Energy Landscape and Robustness of a Gene Regulatory Network: Toggle Switch PLoS Comput. Biol. 2007, 3, e60
70. Wang, J.; Xu, L.; Wang, E. Potential Landscape and Flux Framework of Nonequilibrium Networks: Robustness, Dissipation, and Coherence of Biochemical Oscillations Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 12271-12276
71. Sisan, D. R.; Halter, M.; Hubbard, J. B.; Plant, A. L. Predicting Rates of Cell State Change Caused by Stochastic Fluctuations Using a Data-Driven Landscape Model Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 19262-19267
72. Zhou, J. X.; Aliyu, M.; Aurell, E.; Huang, S. Quasi-Potential Landscape in Complex Multi- Stable Systems J. R. Soc. Interface 2012, 9, 3539-3553
73. Mel'Niko, V. The Kramers Problem: Fifty Years of Development Phys. Rep. 1991, 209, 1-71
74. Han, B.; Wang, J. Least Dissipation Cost as a Design Principle for Robustness and Function of Cellular Networks Phys. Rev. E 2008, 77, 031922
75. Qi, H.; Blanchard, A.; Lu, T. Engineered Genetic Information Processing Circuits WIREs Syst. Biol. Med. 2013, 5, 273-287
76. Becskei, A.; Serrano, L. Engineering Stability in Gene Networks by Autoregulation Nature (London) 2000, 405, 590-593
77. Acar, M.; Becskei, A.; van Oudenaarden, A. Enhancement of Cellular Memory by Reducing Stochastic Transitions Nature (London) 2005, 435, 228-232
78. Xiong, W.; Ferrell, J. E., Jr. A Positive-Feedback-Based Bistable 'Memory Module' that Governs a Cell Fate Decision Nature (London) 2003, 426, 460-465
79. Ferrell, J. E., Jr. Self-Perpetuating States in Signal Transduction: Positive Feedback, Double- Negative Feedback and Bistability Curr. Opin. Chem. Biol. 2002, 6, 140-148
80. Tyson, J. J.; Chen, K. C.; Novak, B. Sniffers, Buzzers, Boggles and Blinkers: Dynamics of Regulatory and Signaling Pathways in the Cell Curr. Opin. Cell Biol. 2003, 15, 221-231
81. Floess, S.; Freyer, J.; Siewert, C.; Baron, U.; Olek, S.; Polansky, J.; Schlawe, K.; Chang, H.- D.; Bopp, T.; Schmitt, E. Epigenetic Control of the Foxp3 Locus in Regulatory T Cells PLoS Biol. 2007, 5, e38
82. Chen, C.; Rowell, E. A.; Thomas, R. M.; Hancock, W. W.; Wells, A. D. Transcriptional Regulation by Foxp3 is Associated with Direct Promoter Occupancy and Modulation of Histone Acetylation J. Biol. Chem. 2006, 281, 36828-36834
83. Huehn, J.; Polansky, J. K.; Hamann, A. Epigenetic Control of FOXP3 Expression: The Key to a Stable Regulatory T-Cell Lineage? Nat. Rev. Immunol. 2009, 9, 83-89
84. Hori, S. Developmental Plasticity of Foxp3+ Regulatory T Cells Curr. Opin. Immunol. 2010, 22, 575-582
85. Xu, W.; Lan, Q.; Chen, M.; Chen, H.; Zhu, N.; Zhou, X.; Wang, J.; Fan, H.; Yan, C.-S.; Kuang, J.-L. Adoptive Transfer of Induced-Treg Cells Effectively Attenuates Murine Airway Allergic Inflammation PLoS ONE 2012, 7, e40314
86. Komanduri, K. V.; Champlin, R. E. Can Treg Therapy Prevent GVHD? Blood 2011, 117, 751-752