A unified design space of synthetic stripe-forming networks

Nature Communications

Volumn 5, Issue , 2014, Pages

  Schaerli, Yolanda ^a,b   Munteanu, Andreea ^a,b   Gili, Magüi ^a,b   Cotterell, James ^a,b   Sharpe, James ^a,b,c   Isalan, Mark ^a,b,d  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSE; BACTERIAL RNA; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; MORPHOGEN;

DESIGN; GENE EXPRESSION; GENETIC ENGINEERING; NETWORK ANALYSIS;

ARTICLE; BACTERIAL STRAIN; COMPUTER MODEL; CONTROLLED STUDY; ESCHERICHIA COLI; GENE REGULATORY NETWORK; GENETIC ENGINEERING; GENOTYPE; NONHUMAN; PHENOTYPE; PLASMID; PROMOTER REGION; PROTEIN EXPRESSION; REPRESSOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SYNTHETIC BIOLOGY; SYNTHETIC STRIPE FORMING NETWORK; THEORETICAL MODEL; BIOLOGICAL MODEL; DNA SEQUENCE; FLUORESCENCE; GENETICS; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROCEDURES;

BASE SEQUENCE; CLONING, MOLECULAR; ESCHERICHIA COLI; FLUORESCENCE; GENE REGULATORY NETWORKS; GENETIC ENGINEERING; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SYNTHETIC BIOLOGY;

EID: 84907765477     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5905     Document Type: Article

References (60)

1. Smolke, C. D. Building outside of the box: iGEM and the BioBricks Foundation. Nat. Biotechnol. 27, 1099-1102 (2009).
2. Shetty, R. P., Endy, D. & Knight, Jr T. F. Engineering BioBrick vectors from BioBrick parts. J. Biol. Eng. 2, 5 (2008).
3. Mutalik, V. K. et al. Precise and reliable gene expression via standard transcription and translation initiation elements. Nat. Methods 10, 354-360 (2013).
4. Mutalik, V. K. et al. Quantitative estimation of activity and quality for collections of functional genetic elements. Nat. Methods 10, 347-353 (2013).
5. Qi, L., Haurwitz, R. E., Shao, W., Doudna, J. A. & Arkin, A. P. RNA processing enables predictable programming of gene expression. Nat. Biotechnol. 30, 1002-1006 (2012).
6. Bashor, C. J. & Collins, J. J. Insulating gene circuits from context by RNA processing. Nat. Biotechnol. 30, 1061-1062 (2012).
7. 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).
8. Payne, S. et al. Temporal control of self-organized pattern formation without morphogen gradients in bacteria. Mol. Syst. Biol. 9, 697 (2013).
9. Bleris, L. et al. Synthetic incoherent feedforward circuits show adaptation to the amount of their genetic template. Mol. Syst. Biol. 7, 519 (2011).
10. Liu, C. et al. Sequential establishment of stripe patterns in an expanding cell population. Science 334, 238-241 (2011).
11. Wang, H. H. et al. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460, 894-898 (2009).
12. Xie, Z., Wroblewska, L., Prochazka, L., Weiss, R. & Benenson, Y. Multi-input RNAi-based logic circuit for identification of specific cancer cells. Science 333, 1307-1311 (2011).
13. Regot, S. et al. Distributed biological computation with multicellular engineered networks. Nature 469, 207-211 (2011).
14. Lohmueller, J. J., Armel, T. Z. & Silver, P. A. A tunable zinc finger-based framework for Boolean logic computation in mammalian cells. Nucleic Acids Res. 40, 5180-5187 (2012).
15. Prindle, A. et al. A sensing array of radically coupled genetic 'biopixels'. Nature 481, 39-44 (2012).
16. Auslander, S., Auslander, D., Muller, M., Wieland, M. & Fussenegger, M. Programmable single-cell mammalian biocomputers. Nature 487, 123-127 (2012).
17. Daniel, R., Rubens, J. R., Sarpeshkar, R. & Lu, T. K. Synthetic analog computation in living cells. Nature 497, 619-623 (2013).
18. Bonnet, J., Yin, P., Ortiz, M. E., Subsoontorn, P. & Endy, D. Amplifying genetic logic gates. Science 340, 599-603 (2013).
19. Moon, T. S., Lou, C., Tamsir, A., Stanton, B. C. & Voigt, C. A. Genetic programs constructed from layered logic gates in single cells. Nature 491, 249-253 (2012).
20. Rodrigo, G., Landrain, T. E. & Jaramillo, A. De novo automated design of small RNA circuits for engineering synthetic riboregulation in living cells. Proc. Natl Acad. Sci. USA 109, 15271-15276 (2012).
21. Cotterell, J. & Sharpe, J. An atlas of gene regulatory networks reveals multiple three-gene mechanisms for interpreting morphogen gradients. Mol. Syst. Biol. 6, 425 (2010).
22. Munteanu, A., Cotterell, J., Sole, R. V. & Sharpe, J. Design principles of stripe-forming motifs: the role of positive feedback. Sci. Rep. 4, 5003 (2014).
23. Isalan, M. Gene networks and liar paradoxes. Bioessays 31, 1110-1115 (2009).
24. Lander, A. D. Morpheus unbound: reimagining the morphogen gradient. Cell 128, 245-256 (2007).
25. Wolpert, L. One hundred years of positional information. Trends Genet. 12, 359-364 (1996).
26. Isalan, M., Lemerle, C. & Serrano, L. Engineering gene networks to emulate Drosophila embryonic pattern formation. PLoS Biol. 3, e64 (2005).
27. Muranaka, N. & Yokobayashi, Y. A synthetic riboswitch with chemical bandpass response. Chem. Commun. (Camb) 46, 6825-6827 (2010).
28. Sohka, T. et al. An externally tunable bacterial band-pass filter. Proc. Natl Acad. Sci. USA 106, 10135-10140 (2009).
29. Sohka, T., Heins, R. A. & Ostermeier, M. Morphogen-defined patterning of Escherichia coli enabled by an externally tunable band-pass filter. J. Biol. Eng. 3, 10 (2009).
30. Kampf, M. M. et al. Rewiring and dosing of systems modules as a design approach for synthetic mammalian signaling networks. Mol. Biosyst. 8, 1824-1832 (2012).
31. Basu, S., Gerchman, Y., Collins, C. H., Arnold, F. H. & Weiss, R. A synthetic multicellular system for programmed pattern formation. Nature 434, 1130-1134 (2005).
32. Entus, R., Aufderheide, B. & Sauro, H. M. Design and implementation of three incoherent feed-forward motif based biological concentration sensors. Syst. Synth. Biol. 1, 119-128 (2007).
33. Greber, D. & Fussenegger, M. An engineered mammalian band-pass network. Nucleic Acids Res. 38, e174 (2010).
34. Ellis, T., Wang, X. & Collins, J. J. Diversity-based, model-guided construction of synthetic gene networks with predicted functions. Nat. Biotechnol. 27, 465-471 (2009).
35. Mangan, S. & Alon, U. Structure and function of the feed-forward loop network motif. Proc. Natl Acad. Sci. USA 100, 11980-11985 (2003).
36. Bintu, L. et al. Transcriptional regulation by the numbers: applications. Curr. Opin. Genet. Dev. 15, 125-135 (2005).
37. Litcofsky, K. D., Afeyan, R. B., Krom, R. J., Khalil, A. S. & Collins, J. J. Iterative plug-and-play methodology for constructing and modifying synthetic gene networks. Nat. Methods 9, 1077-1080 (2012).
38. Guet, C. C., Elowitz, M. B., Hsing, W. & Leibler, S. Combinatorial synthesis of genetic networks. Science 296, 1466-1470 (2002).
39. Schaerli, Y. & Isalan, M. Building synthetic gene circuits from combinatorial libraries: screening and selection strategies. Mol. Biosyst. 9, 1559-1567 (2013).
40. Pedelacq, J. D., Cabantous, S., Tran, T., Terwilliger, T. C. & Waldo, G. S. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 24, 79-88 (2006).
41. Noireaux, V., Bar-Ziv, R. & Libchaber, A. Principles of cell-free genetic circuit assembly. Proc. Natl Acad. Sci. USA 100, 12672-12677 (2003).
42. Shis, D. L. & Bennett, M. R. Library of synthetic transcriptional AND gates built with split T7 RNA polymerase mutants. Proc. Natl Acad. Sci. USA 110, 5028-5033 (2013).
43. Hoffmann, F. & Rinas, U. Stress induced by recombinant protein production in Escherichia coli . Adv. Biochem. Eng. Biotechnol. 89, 73-92 (2004).
44. Gill, R. T., Valdes, J. J. & Bentley, W. E. A comparative study of global stress gene regulation in response to overexpression of recombinant proteins in Escherichia coli . Metab. Eng. 2, 178-189 (2000).
45. Tan, C., Marguet, P. & You, L. Emergent bistability by a growth-modulating positive feedback circuit. Nat. Chem. Biol. 5, 842-848 (2009).
46. Hart, Y. & Alon, U. The utility of paradoxical components in biological circuits. Mol. Cell 49, 213-221 (2013).
47. 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).
48. Rodrigo, G. & Elena, S. F. Structural discrimination of robustness in transcriptional feedforward loops for pattern formation. PLoS ONE 6, e16904 (2011).
49. Slusarczyk, A. L., Lin, A. & Weiss, R. Foundations for the design and implementation of synthetic genetic circuits. Nat. Rev. Genet. 13, 406-420 (2012).
50. Atkinson, M. R., Savageau, M. A., Myers, J. T. & Ninfa, A. J. Development of genetic circuitry exhibiting toggle switch or oscillatory behavior in Escherichia coli. Cell 113, 597-607 (2003).
51. Guido, N. J. et al. A bottom-up approach to gene regulation. Nature 439, 856-860 (2006).
52. Tigges, M., Marquez-Lago, T. T., Stelling, J. & Fussenegger, M. A tunable synthetic mammalian oscillator. Nature 457, 309-312 (2009).
53. Ciliberti, S., Martin, O. C. & Wagner, A. Innovation and robustness in complex regulatory gene networks. Proc. Natl Acad. Sci. USA 104, 13591-13596 (2007).
54. Munteanu, A. & Sole, R. V. Neutrality and robustness in evo-devo: emergence of lateral inhibition. PLoS Comput. Biol. 4, e1000226 (2008).
55. Hsu, C. et al. Stochastic signalling rewires the interaction map of a multiple feedback network during yeast evolution. Nat. Commun. 3, 682 (2012).
56. Guzman, L. M., Belin, D., Carson, M. J. & Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130 (1995).
57. Andersen, J. B. et al. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl. Environ. Microbiol. 64, 2240-2246 (1998).
58. Khlebnikov, A., Datsenko, K. A., Skaug, T., Wanner, B. L. & Keasling, J. D. Homogeneous expression of the P(BAD) promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. Microbiology. 147, 3241-3247 (2001).
59. Kogenaru, M. & Tans, S. J. An improved Escherichia coli strain to host gene regulatory networks involving both the AraC and LacI inducible transcription factors. J. Biol. Eng. 8, 2 (2014).
60. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008 (2006).