Transcriptional regulation with CRISPR-Cas9: Principles, advances, and applications

Current Opinion in Biotechnology

Volumn 40, Issue , 2016, Pages 177-184

  Didovyk, Andriy ^a,b   Borek, Bartłomiej ^a,b   Tsimring, Lev ^a,b   Hasty, Jeff ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b University of California San Diego   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENES;

EASE-OF-USE; EPIGENOMES; GENETIC SCREENING; SYNTHETIC BIOLOGY; TRANSCRIPTIONAL REGULATION; TRANSCRIPTOMES;

METABOLIC ENGINEERING;

CASPASE 9; DNA;

ADAPTIVE IMMUNITY; BIOTECHNOLOGICAL PROCEDURES; CRISPR CAS SYSTEM; GAIN OF FUNCTION MUTATION; GENE REGULATORY NETWORK; HUMAN; LOSS OF FUNCTION MUTATION; METABOLIC ENGINEERING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; REVIEW; RNA EDITING; SYNTHETIC BIOLOGY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; GENE EDITING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS;

ANIMALS; CRISPR-CAS SYSTEMS; GENE EDITING; GENE EXPRESSION REGULATION; HUMANS; TRANSCRIPTION, GENETIC;

EID: 84975475973     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2016.06.003     Document Type: Review

References (70)

1. Brophy J.A.N., Voigt C.A. Principles of genetic circuit design. Nat Methods 2014, 11:508-520.
2. Strauss A., Lahaye T. Zinc fingers TAL effectors, or Cas9-based DNA binding proteins: what's best for targeting desired genome loci?. Mol Plant 2013, 6:1384-1387.
3. Sander J.D., Joung J.K. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 2014, 32:347-355.
4. Marraffini L.A. CRISPR-Cas immunity in prokaryotes. Nature 2015, 526:55-61.
5. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. Programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337:816-821.
6. Gasiunas G., Barrangou R., Horvath P., Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 2012, 109:E2579-E2586.
7. Qi L.S., Larson M.H., Gilbert L.A., Doudna J.A., Weissman J.S., Arkin A.P., Lim W.A. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 2013, 152:1173-1183.
8. Bikard D., Jiang W., Samai P., Hochschild A., Zhang F., Marraffini L.A. Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res 2013, 41:7429-7437.
9. Kuscu C., Arslan S., Singh R., Thorpe J., Adli M. Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat Biotechnol 2014, 32:677-683.
10. Nielsen A.A.K., Voigt C.A. Multi-input CRISPR/Cas genetic circuits that interface host regulatory networks. Mol Syst Biol 2014, 10:763.
11. Didovyk A., Borek B., Hasty J., Tsimring L. Orthogonal modular gene repression in Escherichia coli using engineered CRISPR/Cas9. ACS Synth Biol 2016, 5:81-88.
12. 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., et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 2013, 154:442-451.
13. Farzadfard F., Perli S.D., Lu T.K. Tunable and multi-functional eukaryotic transcription factors based on CRISPR/Cas. ACS Synth Biol 2013, 2:604-613.
14. Kiani S., Beal J., Ebrahimkhani M.R., Huh J., Hall R.N., Xie Z., Li Y., Weiss R. CRISPR transcriptional repression devices and layered circuits in mammalian cells. Nat Methods 2014, 11:723-726.
15. Tong Y., Charusanti P., Zhang L., Weber T., Lee S.Y. CRISPR-Cas9 based engineering of Actinomycetal genomes. ACS Synth Biol 2015, 4:1020-1029.
16. Cleto S., Jensen J.K., Wendisch V.F., Lu T.K. Corynebacterium glutamicum metabolic engineering with CRISPR interference (CRISPRi). ACS Synth Biol 2016, 10.1021/acssynbio.5b00216.
17. Peters J.M., Ph D., Larson M.H., Hawkins J.S., Lu C.H.S., Koo B., Shiver A.L., Whitehead E.H., Weissman J.S., Brown E.D., et al. A comprehensive CRISPR-based functional analysis of essential genes in bacteria. Cell 2016, 10.1016/j.cell.2016.05.003.
18. Wang Y., Zhang Z.-T., Seo S.-O., Lynn P., Lu T., Jin Y.-S., Blaschek H.P. Gene transcription repression in Clostridium beijerinckii using CRISPR-dCas9. Biotechnol Bioeng 2016, 10.1002/bit.26020.
19. Gilbert L.A., Horlbeck M.A., Adamson B., Villalta J.E., Chen Y., Whitehead E.H., Guimaraes C., Panning B., Ploegh H.L., Bassik M.C., et al. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 2014, 159:647-661.
20. Konermann S., Brigham M.D., Trevino A.E., Hsu P.D., Heidenreich M., Cong L., Platt R.J., Scott D.A., Church G.M., Zhang F. Optical control of mammalian endogenous transcription and epigenetic states. Nature 2013, 500:472-476.
21. Piatek A., Ali Z., Baazim H., Li L., Abulfaraj A., Al-Shareef S., Aouida M., Mahfouz M.M. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 2015, 13:578-589.
22. Kearns N.A., Pham H., Tabak B., Genga R.M., Silverstein N.J., Garber M., Maehr R. Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat Methods 2015, 12:401-403.
23. Kearns N.A., Genga R.M.J., Enuameh M.S., Garber M., Wolfe S.A., Maehr R. Cas9 effector-mediated regulation of transcription and differentiation in human pluripotent stem cells. Development 2014, 141:219-223.
24. Zalatan J.G., Lee M.E., Almeida R., Gilbert L.A., Whitehead E.H., La Russa M., Tsai J.C., Weissman J.S., Dueber J.E., Qi L.S., et al. Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell 2015, 160:339-350.
25. Thakore P.I., Ippolito A.M.D., Song L., Safi A., Shivakumar N.K., Kabadi A.M., Reddy T.E., Crawford G.E., Gersbach C.A. Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nat Methods 2015, 12:1143-1149.
26. Chakraborty S., Ji H., Kabadi A.M., Gersbach C.A., Christoforou N., Leong K.W. A CRISPR/Cas9-based system for reprogramming cell lineage specification. Stem Cell Rep 2014, 3:940-947.
27. Hilton I.B., D'Ippolito A.M., Vockley C.M., Thakore P.I., Crawford G.E., Reddy T.E., Gersbach C.A. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 2015, 33:510-517.
28. Mali P., Aach J., Stranges P.B., Esvelt K.M., Moosburner M., Kosuri S., Yang L., Church G.M. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 2013, 31:833-838.
29. Maeder M.L., Linder S.J., Cascio V.M., Fu Y., Ho Q.H., Joung J.K. CRISPR RNA - guided activation of endogenous human genes. Nat Methods 2013, 10:977-981.
30. 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., et al. RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods 2013, 10:973-976.
31. Cheng A.W., Wang H., Yang H., Shi L., Katz Y., Theunissen T.W., Rangarajan S., Shivalila C.S., Dadon D.B., Jaenisch R. Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res 2013, 23:1163-1171.
32. Balboa D., Weltner J., Eurola S., Trokovic R., Wartiovaara K., Otonkoski T. Conditionally stabilized dCas9 activator for controlling gene expression in human cell reprogramming and differentiation. Stem Cell Rep 2015, 5:448-459.
33. Chavez A., Scheiman J., Vora S., Pruitt B.W., Tuttle M., Iyer R.E.P., Lin S., Kiani S., Guzman C.D., Wiegand D.J., et al. Highly efficient Cas9-mediated transcriptional programming. Nat Methods 2015, 12:2-6.
34. Tanenbaum M.E., Gilbert L.A., Qi L.S., Weissman J.S., Vale R.D. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 2014, 159:635-646.
35. Shechner D.M., Hacisuleyman E., Younger S.T., Rinn J.L. Multiplexable, locus-specific targeting of long RNAs with CRISPR-display. Nat Methods 2015, 12:664-670.
36. Konermann S., Brigham M.D., Trevino A.E., Joung J., Abudayyeh O.O., Barcena C., Hsu P.D., Habib N., Gootenberg J.S., Nishimasu H., et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 2015, 517:583-588.
37. System C.C., Zetsche B., Gootenberg J.S., Abudayyeh O.O., Regev A., Koonin E.V., Zhang F., Pam T., Zetsche B., Gootenberg J.S., et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 2015, 163:1-13.
38. Ma H., Naseri A., Reyes-Gutierrez P., Wolfe S.A., Zhang S., Pederson T. Multicolor CRISPR labeling of chromosomal loci in human cells. Proc Natl Acad Sci U S A 2015, 112:3002-3007.
39. Esvelt K.M., Mali P., Braff J.L., Moosburner M., Yaung S.J., Church G.M. Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods 2013, 10:1116-1121.
40. Kleinstiver B.P., Prew M.S., Tsai S.Q., Topkar V.V., Nguyen N.T., Zheng Z., Gonzales A.P.W., Li Z., Peterson R.T., Yeh J.-R.J., et al. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 2015, 523:481-485.
41. Braff J.L., Yaung S.J., Esvelt K.M., Church G.M. Characterization of Cas9-guide RNA Orthologs. Cold Spring Harb Protoc 2016, 2016. pdb.top086793.
42. Chavez A., Tuttle M., Pruitt B.W., Ewen-campen B., Chari R., Ter-ovanesyan D., Haque S.J., Cecchi R.J., Kowal E.J.K., Buchthal J., et al. Comparison of Cas9 activators in multiple species. Nat Methods 2016, 10.1038/nmeth.3871.
43. Cradick T.J., Qiu P., Lee C.M., Fine E.J., Bao G. COSMID: a web-based tool for identifying and validating CRISPR/Cas off-target sites. Mol Ther Nucleic Acids 2014, 3:e214.
44. Lin Y., Cradick T.J., Brown M.T., Deshmukh H., Ranjan P., Sarode N., Wile B.M., Vertino P.M., Stewart F.J., Bao G. CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res 2014, 42:7473-7485.
45. Richardson C.D., Ray G.J., DeWitt M.A., Curie G.L., Corn J.E. Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat Biotechnol 2016, 34.
46. Knight S.C., Xie L., Deng W., Guglielmi B., Witkowsky L.B., Bosanac L., Zhang E.T., El Beheiry M., Masson J.-B., Dahan M., et al. Dynamics of CRISPR-Cas9 genome interrogation in living cells. Science 2015, 350:823-826.
47. Sternberg S.H., LaFrance B., Kaplan M., Doudna J.A. Conformational control of DNA target cleavage by CRISPR-Cas9. Nature 2015, 527:110-113.
48. Kiani S., Chavez A., Tuttle M., Hall R.N., Chari R., Ter-Ovanesyan D., Qian J., Pruitt B.W., Beal J., Vora S., et al. Cas9 gRNA engineering for genome editing, activation and repression. Nat Methods 2015, 12:1051-1054.
49. Cress B.F., Jones J.A., Kim D.C., Leitz Q.D., Englaender J.A., Collins S.M., Linhardt R.J., Koffas M.A.G. Rapid generation of CRISPR/dCas9-regulated, orthogonally repressible hybrid T7-lac promoters for modular, tuneable control of metabolic pathway fluxes in Escherichia coli. Nucleic Acids Res 2016, 10.1093/nar/gkw231.
50. Mekler V., Minakhin L., Semenova E., Kuznedelov K., Severinov K. Kinetics of the CRISPR-Cas9 effector complex assembly and the role of 3'-terminal segment of guide RNA. Nucleic Acids Res 2016, 44:2837-2845.
51. Moreno-Mateos M.A., Vejnar C.E., Beaudoin J.-D., Fernandez J.P., Mis E.K., Khokha M.K., Giraldez A.J. CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo. Nat Methods 2015, 12:982-988.
52. Singh R., Kuscu C., Quinlan a., Qi Y., Adli M. Cas9-chromatin binding information enables more accurate CRISPR off-target prediction. Nucleic Acids Res 2015, 43:1-8.
53. Kleinstiver B.P., Pattanayak V., Prew M.S., Tsai S.Q., Nguyen N.T., Zheng Z., Keith Joung J. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 2016, 529:490-495.
54. Slaymaker I.M., Gao L., Zetsche B., Scott D.A., Yan W.X., Zhang F. Rationally engineered Cas9 nucleases with improved specificity. Science 2016, 351:84-88.
55. Heigwer F., Kerr G., Boutros M. E-CRISP: fast CRISPR target site identification. Nat Methods 2014, 11:122-123.
56. Hasty J., McMillen D., Collins J.J. Engineered gene circuits. Nature 2002, 420:224-230.
57. Nissim L., Perli S.D., Fridkin A., Perez-Pinera P., Lu T.K. Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol Cell 2014, 54:698-710.
58. Gao Y., Zhao Y. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J Integr Plant Biol 2014, 56:343-349.
59. Liu Y., Zeng Y., Liu L., Zhuang C., Fu X., Huang W., Cai Z. Synthesizing AND gate genetic circuits based on CRISPR-Cas9 for identification of bladder cancer cells. Nat Commun 2014, 5:5393.
60. Sternberg S.H., Redding S., Jinek M., Greene E.C., Doudna J. a: DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 2014, 507:62-67.
61. Josephs E.A., Kocak D.D., Fitzgibbon C.J., McMenemy J., Gersbach C.A., Marszalek P.E. Structure and specificity of the RNA-guided endonuclease Cas9 during DNA interrogation, target binding and cleavage. Nucleic Acids Res 2015, 43:8924-8941.
62. Khakhar A., Bolten N.J., Nemhauser J., Klavins E. Cell-cell communication in yeast using auxin biosynthesis and auxin responsive CRISPR transcription factors. ACS Synth Biol 2016, 5:279-286.
63. Shalem O., Sanjana N.E., Zhang F. High-throughput functional genomics using CRISPR-Cas9. Nat Rev Genet 2015, 16:299-311.
64. Agrotis A., Ketteler R. A new age in functional genomics using CRISPR/Cas9 in arrayed library screening. Front Genet 2015, 6:1-15.
65. Jakočiunas T., Bonde I., Herrgård M., Harrison S.J., Kristensen M., Pedersen L.E., Jensen M.K., Keasling J.D. Multiplex metabolic pathway engineering using CRISPR/Cas9 in Saccharomyces cerevisiae. Metab Eng 2015, 28:213-222.
66. Lv L., Ren Y.-L., Chen J.-C., Wu Q., Chen G.-Q. Application of CRISPRi for prokaryotic metabolic engineering involving multiple genes, a case study: controllable P(3HB-co-4HB) biosynthesis. Metab Eng 2015, 29:160-168.
67. Cress B.F., Toparlak ÖD, Guleria S., Lebovich M., Stieglitz J.T., Englaender J.A., Jones J.A., Linhardt R.J., Koffas M.A.G. CRISPathBrick: modular combinatorial assembly of type II-A CRISPR arrays for dCas9-mediated multiplex transcriptional repression in E. coli. ACS Synth Biol 2015, 4:987-1000.
68. Díaz E. Bacterial degradation of aromatic pollutants: a paradigm of metabolic versatility. Int Microbiol 2004, 7:173-180.
69. Checa S.K., Zurbriggen M.D., Soncini F.C. Bacterial signaling systems as platforms for rational design of new generations of biosensors. Curr Opin Biotechnol 2012, 23:766-772.
70. Jia H., Fan Y., Feng X., Li C. Enhancing stress-resistance for efficient microbial biotransformations by synthetic biology. Front Bioeng Biotechnol 2014, 2:44.