Negative autoregulation matches production and demand in synthetic transcriptional networks

ACS Synthetic Biology

Volumn 3, Issue 8, 2014, Pages 589-599

  Franco, Elisa ^a   Giordano, Giulia ^b   Forsberg, Per Ola ^c   Murray, Richard M ^d  

^a University of California Riverside   (United States)

^b UNIVERSITY OF UDINE   (Italy)

^c CENTRAL HOSPITAL   (Sweden)

^d California Institute of Technology   (United States)

Author keywords

in vitro; negative feedback; nucleic acid systems; synthetic biology; transcriptional circuits

Indexed keywords

ARTICLE; AUTOREGULATION; COMPUTER PROGRAM; GENE; IN VITRO STUDY; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; POSITIVE FEEDBACK; PRIORITY JOURNAL; RESPONSE TIME; RNA TRANSCRIPTION; SYNTHETIC BIOLOGY; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; HOMEOSTASIS; PROCEDURES; SYSTEMS BIOLOGY;

FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HOMEOSTASIS; MODELS, GENETIC; SYSTEMS BIOLOGY; TRANSCRIPTION, GENETIC;

EID: 84906230280     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb400157z     Document Type: Article

References (54)

1. Purnick, P. E. and Weiss, R. (2009) The second wave of synthetic biology: From modules to systems Nat. Rev. Mol. Cell Biol. 10, 410-422
2. Dong, H., Nilsson, L., and Kurland, C. G. (1995) Gratuitous overexpression of genes in Escherichia coli leads to growth inhibition and ribosome destruction J. Bacteriol. 177, 1497-1504
3. Scott, M., Gunderson, C. W., Mateescu, E. M., Zhang, Z., and Hwa, T. (2010) Interdependence of cell growth and gene expression: Origins and consequences Science 330, 1099-1102
4. Dunlop, M. J. (2011) Engineering microbes for tolerance to next-generation biofuels Biotechnol. Biofuels 4, 32
5. Pitera, D. J., Paddon, C. J., Newman, J. D., and Keasling, J. D. (2007) Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli Metab. Eng. 9, 193-207
6. Afonin, K. A., Bindewald, E., Yaghoubian, A. J., Voss, N., Jacovetty, E., Shapiro, B. A., and Jaeger, L. (2010) In vitro assembly of cubic RNA-based scaffolds designed in silico Nat. Nanotechnol. 5, 676-682
7. Delebecque, C. J., Lindner, A. B., Silver, P. A., and Aldaye, F. A. (2011) Organization of intracellular reactions with rationally designed RNA assemblies Science 333, 470-474
8. Åstrom, K. J. and Murray, R. (2010) Feedback Systems: An Introduction for Scientists and Engineers, Princeton University Press, Princeton, NJ.
9. Shen-Orr, S. S., Milo, R., Mangan, S., and Alon, U. (2002) Network motifs in the transcriptional regulation network of Escherichia coli Nat. Genet. 31, 64-68
10. Alon, U. (2007) An Introduction to Systems Biology: Design Principles of Biological Circuits, Chapman & Hall/CRC, Boca Raton, FL.
11. Savageau, M. A. (1977) Design of molecular control mechanisms and the demand for gene expression Proc. Natl. Acad. Sci. 74, 5647-5651
12. Shinar, G., Dekel, E., Tlusty, T., and Alon, U. (2006) Rules for biological regulation based on error minimization Nature 103, 3999-4004
13. Becskei, A. and Serrano, L. (2000) Engineering stability in gene networks by autoregulation Nature 405, 590-593
14. Austin, D., Allen, M., McCollum, J., Dar, R., Wilgus, J., Sayler, G., Samatova, N., Cox, C., and Simpson, M. (2006) Gene network shaping of inherent noise spectra Nature 439, 608-611
15. Nevozhay, D., Adams, R. M., Murphy, K. F., Josić, K., and Balázsi, G. (2009) Negative autoregulation linearizes the dose-response and suppresses the heterogeneity of gene expression Proc. Natl. Acad. Sci. 106, 5123-5128
16. Denby, C. M., Im, J. H., Richard, C. Y., Pesce, C. G., and Brem, R. B. (2012) Negative feedback confers mutational robustness in yeast transcription factor regulation Proc. Natl. Acad. Sci. 109, 3874-3878
17. Rosenfeld, N., Elowitz, M. B., and Alon, U. (2002) Negative autoregulation speeds the response times of transcription networks J. Mol. Biol. 323, 785-793
18. Deans, T. L., Cantor, C. R., and Collins, J. J. (2007) A tunable genetic switch based on RNAi and repressor proteins for regulating gene expression in mammalian cells Cell 130, 363-372
19. Shimoga, V., White, J. T., Li, Y., Sontag, E., and Bleris, L. (2013) Synthetic mammalian transgene negative autoregulation Mol. Syst. Biol. 9, 1
20. Kim, J., White, K. S., and Winfree, E. (2006) Construction of an in vitro bistable circuit from synthetic transcriptional switches Mol. Syst. Biol. 1, 68
21. Karig, D. K., Iyer, S., Simpson, M. L., and Doktycz, M. J. (2012) Expression optimization and synthetic gene networks in cell-free systems Nucleic Acids Res. 40, 3763-3774
22. Mori, Y., Nakamura, Y., and Ohuchi, S. (2012) Inhibitory RNA aptamer against SP6 RNA polymerase Biochem. Biophys. Res. Commun. 420, 440-443
23. Kim, J. and Winfree, E. (2011) Synthetic in vitro transcriptional oscillators Mol. Syst. Biol. 7, 465
24. Franco, E., Friedrichs, E., Kim, J., Jungmann, R., Murray, R., Winfree, E., and Simmel, F. C. (2011) Timing molecular motion and production with a synthetic transcriptional clock Proc. Natl. Acad. Sci. 108, E784-E793
25. Hockenberry, A. J. and Jewett, M. C. (2012) Synthetic in vitro circuits Curr. Opin. Chem. Biol. 16, 253-259
26. Markham, N. R. and Zuker, M. (2008) UNAFold software for nucleic acid folding and hybridization Methods Mol. Biol. 453, 3-31
27. Zadeh, J. N., Steenberg, C. D., Bois, J. S., Wolfe, B. R., Pierce, M. B., Khan, A. R., Dirks, R. M., and Pierce, N. A. (2011) NUPACK: Analysis of nucleic acid systems J. Comput. Chem. 32, 170-173
28. Franco, E., Forsberg, P.-O., and Murray, R. M. (2008) Design, modeling and synthesis of an in vitro transcription rate regulatory circuit American Control Conference, 2008 2786-2791 10.1109/ACC.2008.4586915
29. Franco, E. and Murray, R. M. (2008) Design and performance of in vitro transcription rate regulatory circuits 47th IEEE Conference on Decision and Control 161-166
30. Giordano, G., Franco, E., and Murray, R. M. (2013) Feedback architectures to regulate flux of components in artificial gene networks American Control Conference 4747-4752
31. Franco, E. (2012) Analysis, design, and in vitro implementation of robust biochemical networks. Ph.D. thesis, California Institute of Technology.
32. Qian, L. and Winfree, E. (2011) Scaling up digital circuit computation with DNA strand displacement cascades Science 3, 1196-1201
33. Zhang, D. Y., Hariadi, R. F., Choi, H. M., and Winfree, E. (2013) Integrating DNA strand-displacement circuitry with DNA tile self-assembly Nat. Commun. 4, 1965
34. Del Vecchio, D., Ninfa, A., and Sontag, E. (2008) Modular cell biology: Retroactivity and insulation Mol. Syst. Biol. 4, 161
35. Bonacci, W., Teng, P. K., Afonso, B., Niederholtmeyer, H., Grob, P., Silver, P. A., and Savage, D. F. (2012) Modularity of a carbon-fixing protein organelle Proc. Natl. Acad. Sci. 109, 478-483
36. Yurke, B. and Mills, A. P. (2003) Using DNA to power nanostructures Genetic Programming and Evolvable Machines 4, 111-122
37. Zuker, M. and Stiegler, P. (1981) Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information Nucleic Acids Res. 9, 133-148
38. Lee, S. K., Chou, H., Ham, T. S., Lee, T. S., and Keasling, J. D. (2008) Metabolic engineering of microorganisms for biofuels production: From bugs to synthetic biology to fuels Curr. Opin. Biotechnol. 19, 556-563
39. Xie, Z., Liu, S. J., Bleris, L., and Benenson, Y. (2010) Logic integration of mRNA signals by an RNAi-based molecular computer Nucleic Acids Res. 38, 2692-2701
40. Kaplan, S., Bren, A., Dekel, E., and Alon, U. (2008) The incoherent feed-forward loop can generate non-monotonic input functions for genes Mol. Syst. Biol. 4, 1
41. Mangan, S., Zaslaver, A., and Alon, U. (2003) The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks J. Mol. Biol. 334, 197-204
42. Bishop, J. D. and Klavins, E. (2012) Characterization of a biomolecular fuel delivery device under load. 51st IEEE Conference on Decision and Control 3589-3594
43. Soloveichik, D., Seelig, G., and Winfree, E. (2010) DNA as a universal substrate for chemical kinetics Proc. Natl. Acad. Sci. 107, 5393-5398
44. Chen, Y.-J., Dalchau, N., Srinivas, N., Phillips, A., Cardelli, L., Soloveichik, D., and Seelig, G. (2013) Programmable chemical controllers made from DNA Nat. Nanotechnol. 8, 755-762
45. Alon, U. (2007) Network motifs: theory and experimental approaches Nat. Rev. Genet. 8, 450-461
46. Subsoontorn, P., Kim, J., and Winfree, E. (2012) Ensemble Bayesian analysis of bistability in a synthetic transcriptional switch ACS Synth. Biol. 1, 299-316
47. Kim, J. and Murray, R. M. (2011) Analysis and design of a synthetic transcriptional network for exact adaptation IEEE Biomedical Circuits and Systems Conference (BioCAS) 345-348
48. Zhang, D. Y. and Seelig, G. (2011) Dynamic DNA nanotechnology using strand-displacement reactions Nature Chem. 3, 103-113
49. Stoltenburg, R., Reinemann, C., and Strehlitz, B. (2007) SELEX-A (r)evolutionary method to generate high-affinity nucleic acid ligands Biomol. Eng. 24, 381-403
50. Ellington, A. D. and Szostak, J. W. (1990) In vitro selection of RNA molecules that bind specific ligands Nature 346, 818-822
51. Montagne, K., Plasson, R., Sakai, Y., Fujii, T., and Rondelez, Y. (2011) Programming an in vitro DNA oscillator using a molecular networking strategy Mol. Syst. Biol. 7, 1
52. Weitz, M., Kim, J., Kapsner, K., Winfree, E., Franco, E., and Simmel, F. C. (2014) Diversity in the dynamical behaviour of a compartmentalized programmable biochemical oscillator Nat. Chem. 10.1038/nchem.1869
53. Hsiao, V., de los Santos, E. L., Whitaker, W. R., Dueber, J. E., and Murray, R. M. (2013) Design and implementation of a synthetic biomolecular concentration tracker bioRxiv 10.1101/000448
54. de los Santos, E., Hsiao, V., and Murray, R. (2013) Design and implementation of a biomolecular circuit for tracking protein concentration American Control Conference 2290-2294