Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds

Cell

Volumn 160, Issue 1-2, 2015, Pages 339-350

  Zalatan, Jesse G ^a,b,f   Lee, Michael E ^c,d   Almeida, Ricardo ^a,b   Gilbert, Luke A ^a,b,d   Whitehead, Evan H ^a,b,g   La Russa, Marie ^a,b,g   Tsai, Jordan C ^a,b   Weissman, Jonathan S ^a,b,d,e   Dueber, John E ^c,d   Qi, Lei S ^a,b,e,g   Lim, Wendell A ^a,b,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of California at Berkeley   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

^g Stanford University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; DCAS9 PROTEIN; GUIDE RNA; MOLECULAR SCAFFOLD; PROTEIN; RNA BINDING PROTEIN; SMALL CYTOPLASMIC RNA; SYNTHETIC DNA; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CELL FATE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DOWN REGULATION; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; RNA STABILITY; STREPTOCOCCUS PYOGENES; TRANSCRIPTION INITIATION; YEAST; YEAST CELL; CRISPR CAS SYSTEM; GENETIC PROCEDURES; GENETICS; HEK293 CELL LINE; METABOLIC ENGINEERING; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

CRISPR-CAS SYSTEMS; GENE EXPRESSION; GENETIC TECHNIQUES; HEK293 CELLS; HUMANS; METABOLIC ENGINEERING; RNA, GUIDE; SACCHAROMYCES CEREVISIAE; STREPTOCOCCUS PYOGENES;

EID: 84920992414     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.11.052     Document Type: Article

References (49)

1. P.K. Ajikumar, W.-H. Xiao, K.E.J. Tyo, Y. Wang, F. Simeon, E. Leonard, O. Mucha, T.H. Phon, B. Pfeifer, and G. Stephanopoulos Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli Science 330 2010 70 74
2. H. Alper, J. Moxley, E. Nevoigt, G.R. Fink, and G. Stephanopoulos Engineering yeast transcription machinery for improved ethanol tolerance and production Science 314 2006 1565 1568
3. M. Andronescu, A.P. Fejes, F. Hutter, H.H. Hoos, and A. Condon A new algorithm for RNA secondary structure design J. Mol. Biol. 336 2004 607 624
4. R.R. Beerli, D.J. Segal, B. Dreier, and C.F. Barbas III 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. USA 95 1998 14628 14633
5. S.S.-K. Chan, and M. Kyba What is a Master Regulator? J. Stem Cell Res. Ther. 3 2013 114
6. J.A. Chao, Y. Patskovsky, S.C. Almo, and R.H. Singer Structural basis for the coevolution of a viral RNA-protein complex Nat. Struct. Mol. Biol. 15 2008 103 105
7. B. Chen, L.A. Gilbert, B.A. Cimini, J. Schnitzbauer, W. Zhang, G.-W. Li, J. Park, E.H. Blackburn, J.S. Weissman, L.S. Qi, and B. Huang Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system Cell 155 2013 1479 1491
8. P. Daran-Lapujade, S. Rossell, W.M. van Gulik, M.A.H. Luttik, M.J.L. de Groot, M. Slijper, A.J.R. Heck, J.-M. Daran, J.H. de Winde, and H.V. Westerhoff The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels Proc. Natl. Acad. Sci. USA 104 2007 15753 15758
9. C.J. Delebecque, A.B. Lindner, P.A. Silver, and F.A. Aldaye Organization of intracellular reactions with rationally designed RNA assemblies Science 333 2011 470 474
10. J.E. DiCarlo, J.E. Norville, P. Mali, X. Rios, J. Aach, and G.M. Church Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems Nucleic Acids Res. 41 2013 4336 4343
11. J. Du, Y. Yuan, T. Si, J. Lian, and H. Zhao Customized optimization of metabolic pathways by combinatorial transcriptional engineering Nucleic Acids Res. 40 2012 e142
12. K.M. Esvelt, P. Mali, J.L. Braff, M. Moosburner, S.J. Yaung, and G.M. Church Orthogonal Cas9 proteins for RNA-guided gene regulation and editing Nat. Methods 10 2013 1116 1121
13. T. Gaj, C.A. Gersbach, and C.F. Barbas III ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering Trends Biotechnol. 31 2013 397 405
14. L.A. Gilbert, M.H. Larson, L. Morsut, Z. Liu, G.A. Brar, S.E. Torres, N. Stern-Ginossar, O. Brandman, E.H. Whitehead, and J.A. Doudna CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes Cell 154 2013 442 451
15. L.A. Gilbert, M.A. Horlbeck, B. Adamson, J.E. Villalta, Y. Chen, E.H. Whitehead, C. Guimaraes, B. Panning, H.L. Ploegh, and M.C. Bassik Genome-Scale CRISPR-Mediated Control of Gene Repression and Activation Cell 159 2014 647 661
16. M.C. Good, J.G. Zalatan, and W.A. Lim Scaffold proteins: hubs for controlling the flow of cellular information Science 332 2011 680 686
17. A.C. Groner, S. Meylan, A. Ciuffi, N. Zangger, G. Ambrosini, N. Dénervaud, P. Bucher, and D. Trono KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading PLoS Genet. 6 2010 e1000869
18. S. Hattman Unusual transcriptional and translational regulation of the bacteriophage Mu mom operon Pharmacol. Ther. 84 1999 367 388
19. I. Hirao, M. Spingola, D. Peabody, and A.D. Ellington The limits of specificity: an experimental analysis with RNA aptamers to MS2 coat protein variants Mol. Divers. 4 1998-1999 75 89
20. T. Hoshino Violacein and related tryptophan metabolites produced by Chromobacterium violaceum: biosynthetic mechanism and pathway for construction of violacein core Appl. Microbiol. Biotechnol. 91 2011 1463 1475
21. M. Jinek, K. Chylinski, I. Fonfara, M. Hauer, J.A. Doudna, and E. Charpentier A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337 2012 816 821
22. M. Jinek, F. Jiang, D.W. Taylor, S.H. Sternberg, E. Kaya, E. Ma, C. Anders, M. Hauer, K. Zhou, and S. Lin Structures of Cas9 endonucleases reveal RNA-mediated conformational activation Science 343 2014 1247997
23. A.M. Kabadi, and C.A. Gersbach Engineering synthetic TALE and CRISPR/Cas9 transcription factors for regulating gene expression Methods 69 2014 188 197
24. J.D. Keasling Synthetic biology and the development of tools for metabolic engineering Metab. Eng. 14 2012 189 195
25. A.J. Keung, C.J. Bashor, S. Kiriakov, J.J. Collins, and A.S. Khalil Using targeted chromatin regulators to engineer combinatorial and spatial transcriptional regulation Cell 158 2014 110 120
26. L.N. Latimer, M.E. Lee, D. Medina-Cleghorn, R.A. Kohnz, D.K. Nomura, and J.E. Dueber Employing a combinatorial expression approach to characterize xylose utilization in Saccharomyces cerevisiae Metab. Eng. 25 2014 20 29
27. M.E. Lee, A. Aswani, A.S. Han, C.J. Tomlin, and J.E. Dueber Expression-level optimization of a multi-enzyme pathway in the absence of a high-throughput assay Nucleic Acids Res. 41 2013 10668 10678
28. F. Lim, and D.S. Peabody Mutations that increase the affinity of a translational repressor for RNA Nucleic Acids Res. 22 1994 3748 3752
29. F. Lim, T.P. Downey, and D.S. Peabody Translational repression and specific RNA binding by the coat protein of the Pseudomonas phage PP7 J. Biol. Chem. 276 2001 22507 22513
30. P.T. Lowary, and O.C. Uhlenbeck An RNA mutation that increases the affinity of an RNA-protein interaction Nucleic Acids Res. 15 1987 10483 10493
31. P. Mali, J. Aach, P.B. Stranges, K.M. Esvelt, M. Moosburner, S. Kosuri, L. Yang, and G.M. Church CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering Nat. Biotechnol. 31 2013 833 838
32. P. Mali, K.M. Esvelt, and G.M. Church Cas9 as a versatile tool for engineering biology Nat. Methods 10 2013 957 963
33. J.F. Margolin, J.R. Friedman, W.K. Meyer, H. Vissing, H.J. Thiesen, and F.J. Rauscher III Krüppel-associated boxes are potent transcriptional repression domains Proc. Natl. Acad. Sci. USA 91 1994 4509 4513
34. H. Nishimasu, F.A. Ran, P.D. Hsu, S. Konermann, S.I. Shehata, N. Dohmae, R. Ishitani, F. Zhang, and O. Nureki Crystal structure of Cas9 in complex with guide RNA and target DNA Cell 156 2014 935 949
35. C.J. Paddon, P.J. Westfall, D.J. Pitera, K. Benjamin, K. Fisher, D. McPhee, M.D. Leavell, A. Tai, A. Main, and D. Eng High-level semi-synthetic production of the potent antimalarial artemisinin Nature 496 2013 528 532
36. L.S. Qi, M.H. Larson, L.A. Gilbert, J.A. Doudna, J.S. Weissman, A.P. Arkin, and W.A. Lim Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression Cell 152 2013 1173 1183
37. Y. Rais, A. Zviran, S. Geula, O. Gafni, E. Chomsky, S. Viukov, A.A. Mansour, I. Caspi, V. Krupalnik, and M. Zerbib Deterministic direct reprogramming of somatic cells to pluripotency Nature 502 2013 65 70
38. J.L. Rinn, and H.Y. Chang Genome regulation by long noncoding RNAs Annu. Rev. Biochem. 81 2012 145 166
39. D.-K. Ro, E.M. Paradise, M. Ouellet, K.J. Fisher, K.L. Newman, J.M. Ndungu, K.A. Ho, R.A. Eachus, T.S. Ham, and J. Kirby Production of the antimalarial drug precursor artemisinic acid in engineered yeast Nature 440 2006 940 943
40. J.D. Sander, and J.K. Joung CRISPR-Cas systems for editing, regulating and targeting genomes Nat. Biotechnol. 32 2014 347 355
41. R.C. Spitale, M.-C. Tsai, and H.Y. Chang RNA templating the epigenome: long noncoding RNAs as molecular scaffolds Epigenetics 6 2011 539 543
42. F.G. Wulczyn, and R. Kahmann Translational stimulation: RNA sequence and structure requirements for binding of Com protein Cell 65 1991 259 269
43. Y. Yuan, and H. Zhao Directed evolution of a highly efficient cellobiose utilizing pathway in an industrial Saccharomyces cerevisiae strain Biotechnol. Bioeng. 110 2013 2874 2881
44. J.N. Zadeh, C.D. Steenberg, J.S. Bois, B.R. Wolfe, M.B. Pierce, A.R. Khan, R.M. Dirks, and N.A. Pierce NUPACK: Analysis and design of nucleic acid systems J. Comput. Chem. 32 2011 170 173
45. P. Braglia, R. Percudani, and G. Dieci Sequence context effects on oligo(dT) termination signal recognition by Saccharomyces cerevisiae RNA polymerase III J. Biol. Chem. 280 2005 19551 19562
46. Y. Gao, and Y. Zhao Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing J. Integr. Plant Biol. 56 2014 343 349
47. A. Kagansky, H.D. Folco, R. Almeida, A.L. Pidoux, A. Boukaba, F. Simmer, T. Urano, G.L. Hamilton, and R.C. Allshire Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres Science 324 2009 1716 1719
48. -ΔΔC(T) Method Methods 25 2001 402 408
49. J.G. Zalatan, S.M. Coyle, S. Rajan, S.S. Sidhu, and W.A. Lim Conformational control of the Ste5 scaffold protein insulates against MAP kinase misactivation Science 337 2012 1218 1222