Tunable and multifunctional eukaryotic transcription factors based on CRISPR/Cas

ACS Synthetic Biology

Volumn 2, Issue 10, 2013, Pages 604-613

  Farzadfard, Fahim ^a,b,c   Perli, Samuel D ^a,b   Lu, Timothy K ^a,b,c,d  

^a USA   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

CRISPR Cas9; endogenous gene regulation; RNA guided multiplex gene regulation; synthetic biology; synthetic gene regulation; synthetic transcription factors

Indexed keywords

BACTERIAL PROTEIN; DNA; GUIDE RNA; PROTEIN CRISPR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; STREPTOCOCCUS PYOGENES; CRISPR CAS SYSTEM; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLASMID; PROMOTER REGION; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; STREPTOCOCCUS PYOGENES;

BASE SEQUENCE; CRISPR-CAS SYSTEMS; MOLECULAR SEQUENCE DATA; PLASMIDS; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; STREPTOCOCCUS PYOGENES; TRANSCRIPTION FACTORS;

EID: 84886488970     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb400081r     Document Type: Article

References (63)

1. Lelli, K. M., Slattery, M., and Mann, R. S. (2012) Disentangling the many layers of eukaryotic transcriptional regulation Annu. Rev. Genet. 46, 43-68
2. Ellwood, K., Huang, W., Johnson, R., and Carey, M. (1999) Multiple layers of cooperativity regulate enhanceosome-responsive RNA polymerase II transcription complex assembly Mol. Cell. Biol. 19, 2613-2623
3. Chen, L. (1999) Combinatorial gene regulation by eukaryotic transcription factors Curr. Opin. Struct. Biol. 9, 48-55
4. Auslander, S., Auslander, D., Muller, M., Wieland, M., and Fussenegger, M. (2012) Programmable single-cell mammalian biocomputers Nature 487, 123-127
5. Bacchus, W., Lang, M., El-Baba, M. D., Weber, W., Stelling, J., and Fussenegger, M. (2012) Synthetic two-way communication between mammalian cells Nat. Biotechnol. 30, 991-996
6. Bashor, C. J., Horwitz, A. A., Peisajovich, S. G., and Lim, W. A. (2010) Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems Annu. Rev. Biophys. 39, 515-537
7. Nandagopal, N. and Elowitz, M. B. (2011) Synthetic biology: integrated gene circuits Science 333, 1244-1248
8. Guet, C. C., Elowitz, M. B., Hsing, W., and Leibler, S. (2002) Combinatorial synthesis of genetic networks Science 296, 1466-1470
9. Bandyopadhyay, S., Mehta, M., Kuo, D., Sung, M. K., Chuang, R., Jaehnig, E. J., Bodenmiller, B., Licon, K., Copeland, W., Shales, M., Fiedler, D., Dutkowski, J., Guenole, A., van Attikum, H., Shokat, K. M., Kolodner, R. D., Huh, W. K., Aebersold, R., Keogh, M. C., Krogan, N. J., and Ideker, T. (2010) Rewiring of genetic networks in response to DNA damage Science 330, 1385-1389
10. Kwon, E. J., Laderoute, A., Chatfield-Reed, K., Vachon, L., Karagiannis, J., and Chua, G. (2012) Deciphering the transcriptional-regulatory network of flocculation in Schizosaccharomyces pombe PLoS Genet. 8, e1003104
11. Tabor, J. J., Salis, H. M., Simpson, Z. B., Chevalier, A. A., Levskaya, A., Marcotte, E. M., Voigt, C. A., and Ellington, A. D. (2009) A synthetic genetic edge detection program Cell 137, 1272-1281
12. Lou, C., Liu, X., Ni, M., Huang, Y., Huang, Q., Huang, L., Jiang, L., Lu, D., Wang, M., Liu, C., Chen, D., Chen, C., Chen, X., Yang, L., Ma, H., Chen, J., and Ouyang, Q. (2010) Synthesizing a novel genetic sequential logic circuit: a push-on push-off switch Mol. Syst. Biol. 6, 350
13. Leisner, M., Bleris, L., Lohmueller, J., Xie, Z., and Benenson, Y. (2010) Rationally designed logic integration of regulatory signals in mammalian cells Nat. Nanotechnol. 5, 666-670
14. Nissim, L. and Bar-Ziv, R. H. (2010) A tunable dual-promoter integrator for targeting of cancer cells Mol. Syst. Biol. 6, 444
15. Gossen, M. and Bujard, H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters Proc. Natl. Acad. Sci. U.S.A. 89, 5547-5551
16. Belli, G., Gari, E., Piedrafita, L., Aldea, M., and Herrero, E. (1998) An activator/repressor dual system allows tight tetracycline-regulated gene expression in budding yeast Nucl. Acids Res. 26, 942-947
17. Cronin, C. A., Gluba, W., and Scrable, H. (2001) The lac operator-repressor system is functional in the mouse Genes Dev. 15, 1506-1517
18. Urlinger, S., Baron, U., Thellmann, M., Hasan, M. T., Bujard, H., and Hillen, W. (2000) Exploring the sequence space for tetracycline-dependent transcriptional activators: novel mutations yield expanded range and sensitivity Proc. Natl. Acad. Sci. U.S.A. 97, 7963-7968
19. Khalil, A. S., Lu, T. K., Bashor, C. J., Ramirez, C. L., Pyenson, N. C., Joung, J. K., and Collins, J. J. (2012) A synthetic biology framework for programming eukaryotic transcription functions Cell 150, 647-658
20. Li, Y., Moore, R., Guinn, M., and Bleris, L. (2012) Transcription activator-like effector hybrids for conditional control and rewiring of chromosomal transgene expression Sci. Rep. 2, 897
21. Bae, K. H., Kwon, Y. D., Shin, H. C., Hwang, M. S., Ryu, E. H., Park, K. S., Yang, H. Y., Lee, D. K., Lee, Y., Park, J., Kwon, H. S., Kim, H. W., Yeh, B. I., Lee, H. W., Sohn, S. H., Yoon, J., Seol, W., and Kim, J. S. (2003) Human zinc fingers as building blocks in the construction of artificial transcription factors Nat. Biotechnol. 21, 275-280
22. Morbitzer, R., Romer, P., Boch, J., and Lahaye, T. (2010) Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors Proc. Natl. Acad. Sci. U.S.A. 107, 21617-21622
23. Ellis, T., Wang, X., and Collins, J. J. (2009) Diversity-based, model-guided construction of synthetic gene networks with predicted functions Nat. Biotechnol. 27, 465-471
24. Lohmueller, J. J., Armel, T. Z., and Silver, P. A. (2012) A tunable zinc finger-based framework for Boolean logic computation in mammalian cells Nucl. Acids Res. 40, 5180-5187
25. Perez-Pinera, P., Ousterout, D. G., Brunger, J. M., Farin, A. M., Glass, K. A., Guilak, F., Crawford, G. E., Hartemink, A. J., and Gersbach, C. A. (2013) Synergistic and tunable human gene activation by combinations of synthetic transcription factors Nat. Methods 10, 239-242
26. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J. A., Somia, N. V., Bogdanove, A. J., and Voytas, D. F. (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting Nucl. Acids Res. 39, e82
27. Maeder, M. L., Linder, S. J., Reyon, D., Angstman, J. F., Fu, Y., Sander, J. D., and Joung, J. K. (2013) Robust, synergistic regulation of human gene expression using TALE activators Nat. Methods 10, 243-245
28. Sanjana, N. E., Cong, L., Zhou, Y., Cunniff, M. M., Feng, G., and Zhang, F. (2012) A transcription activator-like effector toolbox for genome engineering Nat. Protoc. 7, 171-192
29. Reyon, D., Tsai, S. Q., Khayter, C., Foden, J. A., Sander, J. D., and Joung, J. K. (2012) FLASH assembly of TALENs for high-throughput genome editing Nat. Biotechnol. 30, 460-465
30. Glick, B. R. (1995) Metabolic load and heterologous gene expression Biotechnol. Adv. 13, 247-261
31. Wiedenheft, B., Sternberg, S. H., and Doudna, J. A. (2012) RNA-guided genetic silencing systems in bacteria and archaea Nature 482, 331-338
32. Bhaya, D., Davison, M., and Barrangou, R. (2011) CRISPR/Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation Annu. Rev. Genet. 45, 273-297
33. Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J. R., and Joung, J. K. (2013) Efficient genome editing in zebrafish using a CRISPR/Cas system Nat. Biotechnol. 31, 227-229
34. Dicarlo, J. E., Norville, J. E., Mali, P., Rios, X., Aach, J., and Church, G. M. (2013) Genome engineering in Saccharomyces cerevisiae using CRISPR/Cas systems Nucl. Acids Res. 41, 4336-4343
35. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., and Zhang, F. (2013) Multiplex genome engineering using CRISPR/Cas systems Science 339, 819-823
36. Jiang, W., Bikard, D., Cox, D., Zhang, F., and Marraffini, L. A. (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems Nat. Biotechnol. 31, 233-239
37. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., and Church, G. M. (2013) RNA-guided human genome engineering via Cas9 Science 339, 823-826
38. Cho, S. W., Kim, S., Kim, J. M., and Kim, J. S. (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease Nat. Biotechnol. 31, 230-232
39. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., and Lim, W. A. (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression Cell 152, 1173-1183
40. Bikard, D., Jiang, W., Samai, P., Hochschild, A., Zhang, F., and Marraffini, L. A. (2013) Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system Nucleic Acids Res. 10.1093/nar/gkt520
41. Beerli, R. R., Segal, D. J.,and Dreier, B., (1998) Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks Proc. Natl. Acad. Sci. U.S.A. 95, 14628-14633
42. Li, W. Z. and Sherman, F. (1991) Two types of TATA elements for the CYC1 gene of the yeast Saccharomyces cerevisiae Mol. Cell. Biol. 11, 666-676
43. Guarente, L., Yocum, R. R., and Gifford, P. (1982) A GAL10-CYC1 hybrid yeast promoter identifies the GAL4 regulatory region as an upstream site Proc. Natl. Acad. Sci. U.S.A. 79, 7410-7414
44. Burke, D. H. and Nickens, D. G. (2002) Expressing RNA aptamers inside cells to reveal proteome and ribonome function Brief Funct. Genomic Proteomic 1, 169-188
45. Kuras, L. and Struhl, K. (1999) Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme Nature 399, 609-613
46. Li, X. Y., Virbasius, A., Zhu, X., and Green, M. R. (1999) Enhancement of TBP binding by activators and general transcription factors Nature 399, 605-609
47. Huang, Q., Gong, C., Li, J., Zhuo, Z., Chen, Y., Wang, J., and Hua, Z. C. (2012) Distance and helical phase dependence of synergistic transcription activation in cis-regulatory module PLoS One 7, e31198
48. Kwak, Y. D., Koike, H., and Sugaya, K. (2003) RNA interference with small hairpin RNAs transcribed from a human U6 promoter-driven DNA vector J. Pharmacol. Sci. 93, 214-217
49. Sawadogo, M. and Roeder, R. G. (1985) Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region Cell 43, 165-175
50. Adra, C. N., Boer, P. H., and McBurney, M. W. (1987) Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter Gene 60, 65-74
51. Dorn, A., Bollekens, J., Staub, A., Benoist, C., and Mathis, D. (1987) A multiplicity of CCAAT box-binding proteins Cell 50, 863-872
52. Blake, M. C., Jambou, R. C., Swick, A. G., Kahn, J. W., and Azizkhan, J. C. (1990) Transcriptional initiation is controlled by upstream GC-box interactions in a TATAA-less promoter Mol. Cell. Biol. 10, 6632-6641
53. Yocum, R. R., Hanley, S., West, R., Jr., and Ptashne, M. (1984) Use of lacZ fusions to delimit regulatory elements of the inducible divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae Mol. Cell. Biol. 4, 1985-1998
54. Labbe, S. and Thiele, D. J. (1999) Copper ion inducible and repressible promoter systems in yeast Methods Enzymol. 306, 145-153
55. Raj, A., Peskin, C. S., Tranchina, D., Vargas, D. Y., and Tyagi, S. (2006) Stochastic mRNA synthesis in mammalian cells PLoS Biol. 4, e309
56. Bak, G., Hwang, S. W., Ko, Y., Lee, J., Kim, Y., Kim, K., Hong, S. K., and Lee, Y. (2010) On-off controllable RNA hybrid expression vector for yeast three-hybrid system BMB Rep. 43, 110-114
57. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., and Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337, 816-821
58. Fu, Y., Foden, J. A., Khayter, C., Maeder, M. L., Reyon, D., Joung, J. K., and Sander, J. D. (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells Nat. Biotechnol. 10.1038/nbt.2623
59. Gilbert, L. A., Larson, M. H., Morsut, L., Liu, Z., Brar, G. A., Torres, S. E., Stern-Ginossar, N., Brandman, O., Whitehead, E. H., Doudna, J. A., Lim, W. A., Weissman, J. S., and Qi, L. S. (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes Cell. 154, 442-451
60. Maeder, M. L., Linder, S. J., Cascio, V. M., Fu, Y., Ho, Q. H., and Joung, J. K. (2013) CRISPR RNA-guided activation of endogenous human genes Nat Methods 10.1038/nmeth.2598
61. Perez-Pinera, P., Kocak, D. D., Vockley, C. M., Adler, A. F., Kabadi, A. M., Polstein, L. R., Thakore, P. I., Glass, K. A., Ousterout, D. G., Leong, K. W., Guilak, F., Crawford, G. E., Reddy, T. E., and Gersbach, C. A. (2013) RNA-guided gene activation by CRISPR-Cas9-based transcription factors Nat. Methods 10.1038/nmeth.2600
62. Daniel, R., Rubens, J. R., Sarpeshkar, R., and Lu, T. K. (2013) Synthetic analog computation in living cells Nature 497, 619-623
63. Cheng, A. A. and Lu, T. K. (2012) Synthetic biology: an emerging engineering discipline Annu. Rev. Biomed. Eng. 14, 155-178