MiRNAs confer phenotypic robustness to gene networks by suppressing biological noise

Nature Communications

Volumn 4, Issue , 2013, Pages

  Siciliano, Velia ^a,c   Garzilli, Immacolata ^a,c   Fracassi, Chiara ^a   Criscuolo, Stefania ^a   Ventre, Simona ^a   Di Bernardo, Diego ^a,b  

^a TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; DOXYCYCLINE; MICRORNA; TRANSCRIPTION FACTOR;

CELL ORGANELLE; EXPERIMENTAL STUDY; MATHEMATICAL ANALYSIS; NOISE; PHENOTYPE; PROTEIN; RNA;

ANIMAL CELL; ARTICLE; BIOLOGICAL FUNCTIONS; CELL MATURATION; CELL POPULATION; CHO CELL LINE; FEEDBACK SYSTEM; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE TARGETING; HUMAN; MATHEMATICAL ANALYSIS; MICROFLUIDICS; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; POSITIVE FEEDBACK; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STEADY STATE; STOCHASTIC MODEL; SYNTHETIC BIOLOGY;

MAMMALIA;

ANIMALS; CHO CELLS; CRICETULUS; E2F1 TRANSCRIPTION FACTOR; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENETIC VECTORS; LENTIVIRUS; MICRORNAS; MODELS, GENETIC; PHENOTYPE; PROTEIN BIOSYNTHESIS; STOCHASTIC PROCESSES; SYNTHETIC BIOLOGY; TRANSCRIPTION, GENETIC;

EID: 84885131782     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3364     Document Type: Article

References (50)

1. Inui, M., Martello, G. & Piccolo, S. Microrna control of signal transduction. Nat. Rev. Mol. Cell Biol. 11, 264-275 (2010).
2. Alvarez-Saavedra, E. & Horvitz, H. R. Many families of c. elegans micrornas are not essential for development or viability. Curr. Biol. 20, 367-373 (2010).
3. Miska, E. A. et al. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet. 3, e215\+ (2007).
4. Abbott, A. L. et al. The let-7 microrna family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in caenorhabditis elegans. Dev. Cell 9, 403-414 (2005). (Pubitemid 41235809)
5. Li, X., Cassidy, J. J., Reinke, C. A., Fischboeck, S. & Ca, R. W. A microrna imparts robustness against environmental fluctuation during development. Cell 137, 273-282 (2009).
6. Ebert, M. S. & Sharp, P. A. Roles for micrornas in conferring robustness to biological processes. Cell 149, 515-524 (2012).
7. Hornstein, E. & Shomron, N. Canalization of development by microRNAs. Nat. Genet. 38, S20-S24 (2006).
8. Herranz, H. & Cohen, S. M. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev. 24, 1339-1344 (2010).
9. Chang, X., Liu, Z., Chen, L. & Wang, R. Bistability and oscillations in gene regulation mediated by small noncoding RNAs. PLoS One 6, e17029 (2011).
10. Li, Y., Li, Y., Zhang, H. & Chen, Y. MicroRNA-Mediated positive feedback loop and optimized bistable switch in a cancer network involving miR-17-92. PLoS One 6, e26302 (2011).
11. Yosef, N. & Regev, A. Impulse control: temporal dynamics in gene transcription. Cell 144, 886-896 (2011).
12. Bleris, L. et al. Synthetic incoherent feedforward circuits show adaptation to the amount of their genetic template. Mol. Syst. Biol. 7, 519 (2011).
13. Tsang, J., Zhu, J. & Oudenaarden, A. V. Microrna-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol. Cell 26, 753-767 (2007). (Pubitemid 46856248)
14. Kitano, H. Biological robustness. Nat. Rev. Genet. 5, 826-837 (2004). (Pubitemid 39457498)
15. Arjun, R. & van Oudenaarden, A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226 (2008).
16. Kaern, M., Elston, T. C., Blake, W. J. & Collins, J. J. Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6, 451-464 (2005). (Pubitemid 40733890)
17. Rosenfeld, N., Elowitz, M. B. & Alon, U. Negative autoregulation speeds the response times of transcription networks. J. Mol. Biol. 323, 785-793 (2002). (Pubitemid 35341055)
18. Ozbudak, E. M., Thattai, M., Kurtser, I., Grossman, A. D. & van Oudenaarden, A. Regulation of noise in the expression of a single gene. Nat. Genet. 31, 69-73 (2002).
19. Raj, A., Rifkin, S. A., Andersen, E. & van Oudenaarden, A. Variability in gene expression underlies incomplete penetrance. Nature 463, 913-918 (2010).
20. Martinez, N. J. et al. A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes Dev. 22, 2535-2549 (2008).
21. Lim, W. A., Lee, C. M. & Tang, C. Design principles of regulatory networks: searching for the molecular algorithms of the cell. Mol. Cell 49, 202-212 (2013).
22. Baek, D. et al. The impact of microRNAs on protein output. Nature 455, 64-71 (2008).
23. Brown, B. D. et al. Endogenous microRNA can be broadly exploited to regulate transgene expression according to tissue, lineage and differentiation state. Nat. Biotech. 25, 1457-1467 (2007). (Pubitemid 350233144)
24. Siciliano, V. et al. Construction and modelling of an inducible positive feedback loop stably integrated in a mammalian cell-line. PLoS Comput. Biol. 7, e1002074 (2011).
25. Gardner, T. S., Cantor, C. R. & Collins, J. J. Construction of a genetic toggle switch in escherichia coli. Nature 403, 339-342 (2000). (Pubitemid 30062394)
26. Maeda, Y. T. & Sano, M. Regulatory dynamics of synthetic gene networks with positive feedback. J. Mol. Biol. 359, 1107-1124 (2006). (Pubitemid 43831916)
27. Becskei, A., Séraphin, B. & Serrano, L. Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion. EMBO J. 20, 2528-2535 (2001). (Pubitemid 32452871)
28. Kramer, B. P. et al. An engineered epigenetic transgene switch in mammalian cells. Nat. Biotechnol. 22, 867-870 (2004). (Pubitemid 38886606)
29. Bennett, M. R. & Hasty, J. Microfluidic devices for measuring gene network dynamics in single cells. Nat. Rev. Genet. 10, 628-638 (2009).
30. Singh, A. Negative feedback through mrna provides the best control of geneexpression noise. IEEE Trans Nanobiosci. 10, 194-200 (2011).
31. Osella, M., Bosia, C., Cora', D. & Caselle, M. The role of incoherent microRNAmediated feedforward loops in noise buffering. PLoS Comput. Biol. 7, e1001101 (2011).
32. Blake, W. J., KAErn, M., Cantor, C. R. & Collins, J. J. Noise in eukaryotic gene expression. Nature 422, 633-637 (2003). (Pubitemid 36460419)
33. Rosenfeld, N., Young, J. W., Alon, U., Swain, P. S. & Elowitz, M. B. Accurate prediction of gene feedback circuit behavior from component properties. Mol. Syst. Biol. 3, 143 (2007).
34. Petersen, M. & Wengel, J. Lna: a versatile tool for therapeutics and genomics. Trends. Biotechnol. 21, 74-81 (2003). (Pubitemid 36165007)
35. Chau, A. H., Walter, J. M., Gerardin, J., Tang, C. & Lim, W. A. Designing synthetic regulatory networks capable of self-organizing cell polarization. Cell 151, 320-332 (2012).
36. Acar, M., Becskei, A. & Oudenaarden, A. V. Enhancement of cellular memory by reducing stochastic transitions. Nature 435, 228-232 (2005). (Pubitemid 40685951)
37. Isaacs, F. J., Hasty, J., Cantor, C. R. & Collins, J. J. Prediction and measurement of an autoregulatory genetic module. Proc. Natl Acad. Sci. 100, 7714-7719 (2003). (Pubitemid 36760035)
38. Davidson, E. H. Emerging properties of animal gene regulatory networks. Nature 468, 911-920 (2010).
39. Mehta, P., Mukhopadhyay, R. & Wingreen, N. S. Exponential sensitivity of noise-driven switching in genetic networks. Phys. Biol. 5, 026005\+ (2008).
40. Walczak, A. M., Onuchic, J. N. & Wolynes, P. G. Absolute rate theories of epigenetic stability. Proc. Natl Acad. Sci. USA 102, 18926-18931 (2005). (Pubitemid 43049543)
41. Deans, T. L., Cantor, C. R. & Collins, J. J. A tunable genetic switch based on RNAi and repressor proteins for regulating gene expression in mammalian cells. Cell 130, 363-372 (2007). (Pubitemid 47081136)
42. O'Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V. & Mendell, J. T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839-843 (2005). (Pubitemid 40839736)
43. Sylvestre, Y. et al. An e2f/mir-20a autoregulatory feedback loop. J. Biol. Chem. 282, 2135-2143 (2007). (Pubitemid 47076740)
44. Fong, A. P. et al. Genetic and epigenetic determinants of neurogenesis and myogenesis. Dev. Cell 22, 721-735 (2012).
45. Thayer, M. J. et al. Positive autoregulation of the myogenic determination gene myod1. Cell 58, 241-248 (1989). (Pubitemid 19191406)
46. Gagan, J., Dey, B. K. & Dutta, A. MicroRNAs regulate and provide robustness to the myogenic transcriptional network. Curr. Opin. Pharmacol. 12, 383-388 (2012).
47. Mukherji, S. et al. Micrornas can generate thresholds in target gene expression. Nat. Genet. 43, 854-859 (2011).
48. Amendola, M. et al. Regulated and multiple miRNA and siRNA delivery into primary cells by a lentiviral platform. Mol. Ther. 17, 1039-1052 (2009).
49. Kolnik, M., Tsimring, L. S. & Hasty, J. Vacuum-assisted cell loading enables shear-free mammalian microfluidic culture. Lab Chip 12, 4732-4737 (2012).
50. Maiwald, T. & Timmer, J. Dynamical modeling and multi-experiment fitting with potterswheel. Bioinformatics 24, 2037-2043 (2008).