A bistable genetic switch based on designable DNA-binding domains

Nature Communications

Volumn 5, Issue , 2014, Pages

  Lebar, Tina ^a,b   Bezeljak, Urban ^a   Golob, Anja ^a   Jerala, Miha ^a   Kadunc, Lucija ^a   Pirš, Boštjan ^a   Stražar, Martin ^a,c   Vučko, Dušan ^a   Zupančič, Uroš ^a   Benčina, Mojca ^a,b   Forstnerič, Vida ^a   Gaber, Rok ^a,b   Lonzarić, Jan ^a,b   Majerle, Andreja ^a,b   Oblak, Alja ^a,b   Smole, Anže ^a   Jerala, Roman ^a,b  

^a NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^b EN FIST CENTRE OF EXCELLENCE   (Slovenia)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL BINDING; DNA; NONLINEARITY;

ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DNA BINDING; EPIGENETICS; GENE SWITCHING; GENETIC ENGINEERING; HEK293 CELL LINE; HUMAN; HUMAN CELL; NUCLEAR REPROGRAMMING; OPERATOR GENE; POSITIVE FEEDBACK; STOCHASTIC MODEL; BINDING COMPETITION; BINDING SITE; CELL LINE; CHEMISTRY; CONFOCAL MICROSCOPY; GENETIC EPIGENESIS; METABOLISM; PROCEDURES; PROTEIN TERTIARY STRUCTURE; STATISTICS; THEORETICAL MODEL;

MAMMALIA;

DNA; LUCIFERASE; PROTEIN BINDING;

BINDING SITES; BINDING, COMPETITIVE; CELL LINE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; DNA; EPIGENESIS, GENETIC; GENETIC ENGINEERING; HEK293 CELLS; HUMANS; LUCIFERASES; MICROSCOPY, CONFOCAL; MODELS, THEORETICAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STOCHASTIC PROCESSES;

EID: 84923276880     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6007     Document Type: Article

References (47)

1. Yao, G., Lee, T. J., Mori, S., Nevins, J. R. & You, L. A bistable Rb-E2F switch underlies the restriction point. Nat. Cell Biol. 10, 476-482 (2008).
2. Tyson, J. J., Chen, K. C. & Novak, B. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr. Opin. Cell Biol. 15, 221-231 (2003).
3. Xiong, W. & Ferrell, J. E. A positive-feedback-based bistable "memory module" that governs a cell fate decision. Nature 426, 460-465 (2003).
4. Ferrell, Jr J. E. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science 280, 895-898 (1998).
5. Kim, D., Rath, O., Kolch, W. & Cho, K.-H. A hidden oncogenic positive feedback loop caused by crosstalk between Wnt and ERK pathways. Oncogene 26, 4571-4579 (2007).
6. Eissing, T. et al. Bistability analyses of a caspase activation model for receptorinduced apoptosis. J. Biol. Chem. 279, 36892-36897 (2004).
7. Monod, J. & Jacob, F. Teleonomic mechanisms in cellular metabolism, growth, and differentiation. Cold Spring Harb. Symp. Quant. Biol. 26, 389-401 (1961).
8. Gardner, T. S., Cantor, C. R. & Collins, J. J. Construction of a genetic toggle switch in Escherichia coli. Nature 403, 339-342 (2000).
9. Kramer, B. P. et al. An engineered epigenetic transgene switch in mammalian cells. Nat. Biotechnol. 22, 867-870 (2004).
10. Elowitz, M. B. & Leibler, S. A synthetic oscillatory network of transcriptional regulators. Nature 403, 335-338 (2000).
11. 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).
12. Moon, T. S., Lou, C. B., Tamsir, A., Stanton, B. C. & Voigt, C. A. Genetic programs constructed from layered logic gates in single cells. Nature 491, 249-253 (2012).
13. Garg, A., Lohmueller, J. J., Silver, P. A. & Armel, T. Z. Engineering synthetic TAL effectors with orthogonal target sites. Nucleic Acids Res. 40, 7584-7595 (2012).
14. Cong, L., Zhou, R., Kuo, Y. C., Cunniff, M. & Zhang, F. Comprehensive interrogation of natural TALE DNA-binding modules and transcriptional repressor domains. Nat. Commun. 3, 968 (2012).
15. Zhang, F. et al. Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat. Biotechnol. 29, 149-153 (2011).
16. Cermak, T. et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82 (2011).
17. Gommans, W. M., Haisma, H. J. & Rots, M. G. Engineering zinc finger protein transcription factors: the therapeutic relevance of switching endogenous gene expression on or off at command. J. Mol. Biol. 354, 507-519 (2005).
18. Qi, L. S. et al. Repurposing CRISPR as an RNA-guided platform for sequencespecific control of gene expression. Cell 152, 1173-1183 (2013).
19. Mali, P. et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833-838 (2013).
20. Gilbert, L. a. et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154, 442-451 (2013).
21. Gaber, R. et al. Designable DNA-binding domains enable construction of logic circuits in mammalian cells. Nat. Chem. Biol. 10, 203-208 (2014).
22. Cherry, J. L. & Adler, F. R. How to make a biological switch. J. Theor. Biol. 203, 117-133 (2000).
23. Witzgall, R., O?Leary, E., Leaf, A., Onaldi, D. & Bonventre, J. V. The Kruppel-associated box-A (KRAB-A) domain of zinc finger proteins mediates transcriptional repression. Proc. Natl Acad. Sci. USA 91, 4514-4518 (1994).
24. Kim, J. H. et al. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS ONE 6, e18556 (2011).
25. Weber, W. et al. Macrolide-based transgene control in mammalian cells and mice. Nat. Biotechnol. 20, 901-907 (2002).
26. Fussenegger, M. et al. Streptogramin-based gene regulation systems for mammalian cells. Nat. Biotechnol. 18, 1203-1208 (2000).
27. Mak, A. N.-S., Bradley, P., Cernadas, R. A., Bogdanove, A. J. & Stoddard, B. L. The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335, 716-719 (2012).
28. Deng, D. et al. Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335, 720-723 (2012).
29. Andrecut, M., Halley, J. D., Winkler, D. a. & Huang, S. A general model for binary cell fate decision gene circuits with degeneracy: indeterminacy and switch behavior in the absence of cooperativity. PLoS ONE 6, e19358 (2011).
30. Macia, J., Widder, S. & Sole, R. Why are cellular switches Boolean? General conditions for multistable genetic circuits. J. Theor. Biol. 261, 126-135 (2009).
31. Meckler, J. F. et al. Quantitative analysis of TALE-DNA interactions suggests polarity effects. Nucleic Acids Res. 41, 4118-4128 (2013).
32. Morbitzer, R., Elsaesser, J., Hausner, J. & Lahaye, T. Assembly of custom TALEtype DNA binding domains by modular cloning. Nucleic Acids Res. 39, 5790-5799 (2011).
33. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
34. Weber, E., Gruetzner, R., Werner, S., Engler, C. & Marillonnet, S. Assembly of designer TAL effectors by Golden Gate cloning. PLoS ONE 6, e19722 (2011).
35. Kim, Y. et al. A library of TAL effector nucleases spanning the human genome. Nat. Biotechnol. 31, 251-258 (2013).
36. Munteanu, A., Constante, M., Isalan, M. & Sole, R. V. Avoiding transcription factor competition at promoter level increases the chances of obtaining oscillation. BMC Syst. Biol. 4, 66 (2010).
37. Siegal-Gaskins, D., Mejia-Guerra, M. K., Smith, G. D. & Grotewold, E. Emergence of switch-like behavior in a large family of simple biochemical networks. PLoS Comput. Biol. 7, e1002039 (2011).
38. Tan, C., Marguet, P. & You, L. Emergent bistability by a growth-modulating positive feedback circuit. Nat. Chem. Biol. 5, 842-848 (2009).
39. Chen, D. & Arkin, A. P. Sequestration-based bistability enables tuning of the switching boundaries and design of a latch. Mol. Syst. Biol. 8, 620 (2012).
40. Nissim, L. & Bar-Ziv, R. H. A tunable dual-promoter integrator for targeting of cancer cells. Mol. Syst. Biol. 6, 444 (2010).
41. Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009).
42. Sander, J. D. et al. Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat. Biotechnol. 29, 697-698 (2011).
43. Szulc, J., Wiznerowicz, M., Sauvain, M. O., Trono, D. & Aebischer, P. A versatile tool for conditional gene expression and knockdown. Nat. Methods 3, 109-116 (2006).
44. Sadowski, I., Ma, J., Triezenberg, S. & Ptashne, M. GAL4-VP16 is an unusually potent transcriptional activator. Nature 335, 563-564 (1988).
45. Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A. & Tsien, R. Y. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276, 29188-29194 (2001).
46. Shcherbakova, D. M. & Verkhusha, V. V. Near-infrared fluorescent proteins for multicolor in vivo imaging. Nat. Methods 10, 751-754 (2013).
47. 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).