CRISPR technology is rapidly evolving, and the scope of CRISPR applications is constantly expanding. CRISPR was originally employed for genome editing. Its application was then extended to epigenome editing, karyotype engineering, chromatin imaging, transcriptome, and metabolic pathway engineering. Now, CRISPR technology is being harnessed for genetic circuits engineering, cell signaling sensing, cellular events recording, lineage information reconstruction, gene drive, DNA genotyping, miRNA quantification, in vivo cloning, site-directed mutagenesis, genomic diversification, and proteomic analysis in situ. It has also been implemented in the translational research of human diseases such as cancer immunotherapy, antiviral therapy, bacteriophage therapy, cancer diagnosis, pathogen screening, microbiota remodeling, stem-cell reprogramming, immunogenomic engineering, vaccine development, and antibody production. This review aims to summarize the key concepts of these CRISPR applications in order to capture the current state of play in this fast-moving field. The key mechanisms, strategies, and design principles for each technological advance are also highlighted.
Get full access to this article
View all access options for this article.
References
1.
McNuttM. Breakthrough to genome editing. Science, 2015; 350:144–5. DOI: 10.1126/science.aae0479.
2.
JansenR, EmbdenJD, GaastraW, et al.Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol, 2002; 43:1565–1575. DOI: 10.1046/j.1365-2958.2002.02839.x.
3.
MojicaFJ, Diez-VillasenorC, Garcia-MartinezJ, et al.Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol, 2005; 60:174–182. DOI: 10.1007/s00239-004-0046-3.
4.
BarrangouR, FremauxC, DeveauH, et al.CRISPR provides acquired resistance against viruses in prokaryotes. Science, 2007; 315:1709–1712. DOI: 10.1126/science.1138140.
5.
GarneauJE, DupuisME, VillionM, et al.The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 2010; 468:67–71. DOI: 10.1038/nature09523.
6.
MarraffiniLA, SontheimerEJ. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science, 2008; 322:1843–1845. DOI: 10.1126/science.1165771.
7.
GasiunasG, BarrangouR, HorvathP, et al.Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A, 2012; 109:E2579–2586. DOI: 10.1073/pnas.1208507109.
8.
JinekM, ChylinskiK, FonfaraI, et al.A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 2012; 337:816–821. DOI: 10.1126/science.1225829.
9.
CongL, RanFA, CoxD, et al.Multiplex genome engineering using CRISPR/Cas systems. Science, 2013; 339:819–823. DOI: 10.1126/science.1231143.
10.
MaliP, YangL, EsveltKM, et al.RNA-guided human genome engineering via Cas9. Science, 2013; 339:823–826. DOI: 10.1126/science.1232033.
11.
ChoSW, KimS, KimJM, et al.Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol, 2013; 31:230–232. DOI: 10.1038/nbt.2507.
12.
GajT, GersbachCA, Barbas CF 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol, 2013; 31:397–405. DOI: 10.1016/j.tibtech.2013.04.004.
13.
GuptaRM, MusunuruK. Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR-Cas9. J Clin Invest, 2014; 124:4154–4161. DOI: 10.1172/JCI72992.
14.
MillerJC, TanS, QiaoG, et al.A TALE nuclease architecture for efficient genome editing. Nat Biotechnol, 2011; 29:143–148. DOI: 10.1038/nbt.1755.
15.
LiT, HuangS, JiangWZ, et al.TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucl Acids Res, 2011; 39:359–372. DOI: 10.1093/nar/gkq704.
16.
KimYG, ChaJ, ChandrasegaranS. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A, 1996; 93:1156–1160. DOI: 10.1073/pnas.93.3.1156.
17.
BitinaiteJ, WahDA, AggarwalAK, et al.FokI dimerization is required for DNA cleavage. Proc Natl Acad Sci U S A, 1998; 95:10570–10575.
18.
HolkersM, MaggioI, LiuJ, et al.Differential integrity of TALE nuclease genes following adenoviral and lentiviral vector gene transfer into human cells. Nucl Acids Res, 2013; 41:e6–3. DOI: 10.1093/nar/gks1446.
19.
BrounsSJ, JoreMM, LundgrenM, et al.Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 2008; 321:960–964. DOI: 10.1126/science.1159689.
20.
DeltchevaE, ChylinskiK, SharmaCM, et al.CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 2011; 471:602–607. DOI: 10.1038/nature09886.
21.
SternbergSH, ReddingS, JinekM, et al.DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, 2014; 507:62–67. DOI: 10.1038/nature13011.
22.
AndersC, NiewoehnerO, DuerstA, et al.Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature, 2014; 513:569–573. DOI: 10.1038/nature13579.
23.
RanFA, CongL, YanWX, et al.In vivo genome editing using Staphylococcus aureus Cas9. Nature, 2015; 520:186–191. DOI: 10.1038/nature14299.
24.
KimE, KooT, ParkSW, et al.In vivo genome editing with a small Cas9 orthologue derived from Campylobacter jejuni. Nat Commun, 2017; 8:1450–0. DOI: 10.1038/ncomms14500.
25.
HouZ, ZhangY, PropsonNE, et al.Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc Natl Acad Sci U S A, 2013; 110:15644–15649. DOI: 10.1073/pnas.1313587110.
26.
ZetscheB, GootenbergJS, AbudayyehOO, et al.Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 2015; 163:759–771. DOI: 10.1016/j.cell.2015.09.038.
27.
SapranauskasR, GasiunasG, FremauxC, et al.The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucl Acids Res, 2011; 39:9275–9282. DOI: 10.1093/nar/gkr606.
28.
BolotinA, QuinquisB, SorokinA, et al.Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 2005; 151:2551–2561. DOI: 10.1099/mic.0.28048-0.
29.
DahlmanJE, AbudayyehOO, JoungJ, et al.Orthogonal gene knockout and activation with a catalytically active Cas9 nuclease. Nat Biotechnol, 2015; 33:1159–1161. DOI: 10.1038/nbt.3390.
30.
KianiS, ChavezA, TuttleM, et al.Cas9 gRNA engineering for genome editing, activation and repression. Nat Methods, 2015; 12:1051–1054. DOI: 10.1038/nmeth.3580.
31.
QiLS, LarsonMH, GilbertLA, et al.Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 2013; 152:1173–1183. DOI: 10.1016/j.cell.2013.02.022.
32.
MaederML, LinderSJ, CascioVM, et al.CRISPR RNA-guided activation of endogenous human genes. Nat Methods, 2013; 10:977–979. DOI: 10.1038/nmeth.2598.
33.
GilbertLA, LarsonMH, MorsutL, et al.CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 2013; 154:442–451. DOI: 10.1016/j.cell.2013.06.044.
34.
GilbertLA, HorlbeckMA, AdamsonB, et al.Genome-scale CRISPR-mediated control of gene repression and activation. Cell, 2014; 159:647–661. DOI: 10.1016/j.cell.2014.09.029.
35.
Perez-PineraP, KocakDD, VockleyCM, et al.RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods, 2013; 10:973–976. DOI: 10.1038/nmeth.2600.
36.
HiltonIB, D'IppolitoAM, VockleyCM, et al.Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol, 2015; 33:510–517. DOI: 10.1038/nbt.3199.
37.
ThakorePI, D'IppolitoAM, SongL, et al.Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nat Methods, 2015; 12:1143–1149. DOI: 10.1038/nmeth.3630.
38.
BarrangouR, DoudnaJA. Applications of CRISPR technologies in research and beyond. Nat Biotechnol, 2016; 34:933–941. DOI: 10.1038/nbt.3659.
39.
KomorAC, BadranAH, LiuDR. CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell, 2017; 168:20–36. DOI: 10.1016/j.cell.2016.10.044.
40.
KnottGJ, DoudnaJA. CRISPR-Cas guides the future of genetic engineering. Science, 2018; 361:866–869. DOI: 10.1126/science.aat5011.
41.
HsuPD, LanderES, ZhangF. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 2014; 157:1262–1278. DOI: 10.1016/j.cell.2014.05.010.
42.
WrightAV, NunezJK, DoudnaJA. Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell, 2016; 164:29–44. DOI: 10.1016/j.cell.2015.12.035.
43.
PulecioJ, VermaN, Mejia-RamirezE, et al.CRISPR/Cas9-based engineering of the epigenome. Cell Stem Cell, 2017; 21:431–447. DOI: 10.1016/j.stem.2017.09.006.
44.
ShalemO, SanjanaNE, HartenianE, et al.Genome-scale CRISPR-Cas9 knockout screening in human cells. Science, 2014; 343:84–87. DOI: 10.1126/science.1247005.
45.
RanFA, HsuPD, WrightJ, et al.Genome engineering using the CRISPR-Cas9 system. Nat Protoc, 2013; 8:2281–2308. DOI: 10.1038/nprot.2013.143.
46.
PaquetD, KwartD, ChenA, et al.Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9. Nature, 2016; 533:125–129. DOI: 10.1038/nature17664.
47.
SadhuMJ, BloomJS, DayL, et al.Highly parallel genome variant engineering with CRISPR-Cas9. Nat Genet, 2018; 50:510–514. DOI: 10.1038/s41588-018-0087-y.
48.
DickinsonDJ, WardJD, ReinerDJ, et al.Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods, 2013; 10:1028–1034. DOI: 10.1038/nmeth.2641.
49.
ChenC, FenkLA, de BonoM. Efficient genome editing in Caenorhabditis elegans by CRISPR-targeted homologous recombination. Nucl Acids Res, 2013; 41:e19–3. DOI: 10.1093/nar/gkt805.
50.
LiuY, YangY, KangX, et al.One-step biallelic and scarless correction of a beta-thalassemia mutation in patient-specific iPSCs without drug selection. Mol Ther Nucl Acids, 2017; 6:57–67. DOI: 10.1016/j.omtn.2016.11.010.
51.
Valletta SDO, IatshadH, BartensteinM, et al.ASXL1 mutation correction by CRISPR/Cas9 restores gene function in leukemia cells and increases survival in mouse xenografts. Oncotarget, 2015; 6:44061–44071. DOI: 10.18632/oncotarget.6392.
52.
ZhuH, LauCH, GohSL, et al.Baculoviral transduction facilitates TALEN-mediated targeted transgene integration and Cre/LoxP cassette exchange in human-induced pluripotent stem cells. Nucl Acids Res, 2013; 41:e18–0. DOI: 10.1093/nar/gkt721.
53.
TayFC, TanWK, GohSL, et al.Targeted transgene insertion into the AAVS1 locus driven by baculoviral vector-mediated zinc finger nuclease expression in human-induced pluripotent stem cells. J Gene Med, 2013; 15:384–395. DOI: 10.1002/jgm.2745.
54.
HowdenSE, McCollB, GlaserA, et al.A Cas9 variant for efficient generation of indel-free knockin or gene-corrected human pluripotent stem cells. Stem Cell Reports, 2016; 7:508–517. DOI: 10.1016/j.stemcr.2016.07.001.
55.
PaixA, FolkmannA, GoldmanDH, et al.Precision genome editing using synthesis-dependent repair of Cas9-induced DNA breaks. Proc Natl Acad Sci U S A, 2017; 114:E10745–E10754. DOI: 10.1073/pnas.1711979114.
56.
ChamperJ, LiuJ, OhSY, et al.Reducing resistance allele formation in CRISPR gene drive. Proc Natl Acad Sci U S A, 2018; 115:5522–5527. DOI: 10.1073/pnas.1720354115.
57.
GantzVM, JasinskieneN, TatarenkovaO, et al.Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc Natl Acad Sci U S A, 2015; 112:E6736–6743. DOI: 10.1073/pnas.1521077112.
58.
HammondA, GaliziR, KyrouK, et al.A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat Biotechnol, 2016; 34:78–83. DOI: 10.1038/nbt.3439.
59.
CrowleyEH, ArenaS, LambaS, et al.Targeted knock-in of the polymorphism rs61764370 does not affect KRAS expression but reduces let-7 levels. Hum Mutat, 2014; 35:208–214. DOI: 10.1002/humu.22487.
60.
PhangRZ, TayFC, GohSL, et al.Zinc finger nuclease-expressing baculoviral vectors mediate targeted genome integration of reprogramming factor genes to facilitate the generation of human induced pluripotent stem cells. Stem Cells Transl Med, 2013; 2:935–945. DOI: 10.5966/sctm.2013-0043.
61.
ChuVT, WeberT, GrafR, et al.Efficient generation of Rosa26 knock-in mice using CRISPR/Cas9 in C57BL/6 zygotes. BMC Biotechnol, 2016;16:4. DOI: 10.1186/s12896-016-0234-4.
62.
Perez-PineraP, OusteroutDG, BrownMT, et al.Gene targeting to the ROSA26 locus directed by engineered zinc finger nucleases. Nucl Acids Res, 2012; 40:3741–3752. DOI: 10.1093/nar/gkr1214.
63.
GaudelliNM, KomorAC, ReesHA, et al.Programmable base editing of A*T to G*C in genomic DNA without DNA cleavage. Nature, 2017; 551:464–471. DOI: 10.1038/nature24644.
64.
KomorAC, KimYB, PackerMS, et al.Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature, 2016; 533:420–424. DOI: 10.1038/nature17946.
65.
GapinskeM, LuuA, WinterJ, et al.CRISPR-SKIP: programmable gene splicing with single base editors. Genome Biol, 2018; 19:10–7. DOI: 10.1186/s13059-018-1482-5.
66.
GehrkeJM, CervantesO, ClementMK, et al.An APOBEC3A-Cas9 base editor with minimized bystander and off-target activities. Nat Biotechnol, 2018; 36:977–982. DOI: 10.1038/nbt.4199.
67.
WangX, LiJ, WangY, et al.Efficient base editing in methylated regions with a human APOBEC3A-Cas9 fusion. Nat Biotechnol, 2018; 36:946–949. DOI: 10.1038/nbt.4198.
68.
LiX, WangY, LiuY, et al.Base editing with a Cpf1-cytidine deaminase fusion. Nat Biotechnol, 2018; 36:324–327. DOI: 10.1038/nbt.4102.
69.
KuscuC, ParlakM, TufanT, et al.CRISPR-STOP: gene silencing through base-editing-induced nonsense mutations. Nat Methods, 2017; 14:710–712. DOI: 10.1038/nmeth.4327.
70.
BillonP, BryantEE, JosephSA, et al.CRISPR-mediated base editing enables efficient disruption of eukaryotic genes through induction of STOP codons. Mol Cell, 2017; 67:1068–1079. DOI: 10.1016/j.molcel.2017.08.008.
71.
KimD, BaeS, ParkJ, et al.Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nat Methods, 2015; 12:237–243. DOI: 10.1038/nmeth.3284.
72.
KuscuC, ArslanS, SinghR, et al.Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat Biotechnol, 2014; 32:677–683. DOI: 10.1038/nbt.2916.
73.
TsaiSQ, ZhengZ, NguyenNT, et al.GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol, 2015; 33:187–197. DOI: 10.1038/nbt.3117.
74.
KleinstiverBP, PattanayakV, PrewMS, et al.High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature, 2016; 529:490–495. DOI: 10.1038/nature16526.
75.
SlaymakerIM, GaoL, ZetscheB, et al.Rationally engineered Cas9 nucleases with improved specificity. Science, 2016; 351:84–88. DOI: 10.1126/science.aad5227.
VakulskasCA, DeverDP, RettigGR, et al.A high-fidelity Cas9 mutant delivered as a ribonucleoprotein complex enables efficient gene editing in human hematopoietic stem and progenitor cells. Nat Med, 2018; 24:1216–1224. DOI: 10.1038/s41591-018-0137-0.
78.
KosickiM, TombergK, BradleyA. Repair of double-strand breaks induced by CRISPR-Cas9 leads to large deletions and complex rearrangements. Nat Biotechnol, 2018; 36:765–771. DOI: 10.1038/nbt.4192.
79.
AdikusumaF, PiltzS, CorbettMA, et al.Large deletions induced by Cas9 cleavage. Nature, 2018; 560:E8–E9. DOI: 10.1038/s41586-018-0380-z.
80.
CanverMC, BauerDE, DassA, et al.Characterization of genomic deletion efficiency mediated by clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9 nuclease system in mammalian cells. J Biol Chem, 2014; 289:21312–21324. DOI: 10.1074/jbc.M114.564625.
81.
ZhengQ, CaiX, TanMH, et al.Precise gene deletion and replacement using the CRISPR/Cas9 system in human cells. Biotechniques, 2014; 57:115–124. DOI: 10.2144/000114196.
82.
AdikusumaF, WilliamsN, GrutznerF, et al.Targeted deletion of an entire chromosome using CRISPR/Cas9. Mol Ther, 2017; 25:1736–1738. DOI: 10.1016/j.ymthe.2017.05.021.
EssletzbichlerP, KonopkaT, SantoroF, et al.Megabase-scale deletion using CRISPR/Cas9 to generate a fully haploid human cell line. Genome Res, 2014; 24:2059–2065. DOI: 10.1101/gr.177220.114.
85.
RanFA, HsuPD, LinCY, et al.Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 2013; 154:1380–1389. DOI: 10.1016/j.cell.2013.08.021.
TorresR, MartinMC, GarciaA, et al.Engineering human tumour-associated chromosomal translocations with the RNA-guided CRISPR-Cas9 system. Nat Commun, 2014; 5:396–4. DOI: 10.1038/ncomms4964.
88.
LuoJ, SunX, CormackBP, et al.Karyotype engineering by chromosome fusion leads to reproductive isolation in yeast. Nature, 2018; 560:392–396. DOI: 10.1038/s41586-018-0374-x.
89.
SasanoY, NagasawaK, KaboliS, et al.CRISPR-PCS: a powerful new approach to inducing multiple chromosome splitting in Saccharomyces cerevisiae. Sci Rep, 2016; 6:3027–8. DOI: 10.1038/srep30278.
90.
DiCarloJE, ChavezA, DietzSL, et al.Safeguarding CRISPR-Cas9 gene drives in yeast. Nat Biotechnol, 2015; 33:1250–1255. DOI: 10.1038/nbt.3412.
91.
LiF, ScottMJ. CRISPR/Cas9-mediated mutagenesis of the white and Sex lethal loci in the invasive pest, Drosophila suzukii. Biochem Biophys Res Commun, 2016; 469:911–916. DOI: 10.1016/j.bbrc.2015.12.081.
92.
GantzVM, BierE. Genome editing. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science, 2015; 348:442–444. DOI: 10.1126/science.aaa5945.
93.
McFarlaneGR, WhitelawCBA, LillicoSG. CRISPR-based gene drives for pest control. Trends Biotechnol, 2018; 36:130–133. DOI: 10.1016/j.tibtech.2017.10.001.
94.
KyrouK, HammondAM, GaliziR, et al.A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat Biotechnol, 2018; 36:1062–1066. DOI: 10.1038/nbt.4245.
95.
ShapiroRS, ChavezA, PorterCBM, et al.A CRISPR-Cas9-based gene drive platform for genetic interaction analysis in Candida albicans. Nat Microbiol, 2018; 3:73–82. DOI: 10.1038/s41564-017-0043-0.
96.
YeoNC, ChavezA, Lance-ByrneA, et al.An enhanced CRISPR repressor for targeted mammalian gene regulation. Nat Methods, 2018; 15:611–616. DOI: 10.1038/s41592-018-0048-5.
97.
ThakorePI, KwonJB, NelsonCE, et al.RNA-guided transcriptional silencing in vivo with S. aureus CRISPR-Cas9 repressors. Nat Commun, 2018; 9:167–4. DOI: 10.1038/s41467-018-04048-4.
98.
AmabileA, MigliaraA, CapassoP, et al.Inheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing. Cell, 2016; 167:219–232.e14. DOI: 10.1016/j.cell.2016.09.006.
99.
KearnsNA, PhamH, TabakB, et al.Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat Methods, 2015; 12:401–403. DOI: 10.1038/nmeth.3325.
100.
KwonDY, ZhaoYT, LamonicaJM, et al.Locus-specific histone deacetylation using a synthetic CRISPR-Cas9-based HDAC. Nat Commun, 2017; 8:1531–5. DOI: 10.1038/ncomms15315.
101.
HuangYH, SuJ, LeiY, et al.DNA epigenome editing using CRISPR-Cas SunTag-directed DNMT3A. Genome Biol, 2017; 18:17–6. DOI: 10.1186/s13059-017-1306-z.
102.
PfluegerC, TanD, SwainT, et al.A modular dCas9-SunTag DNMT3A epigenome editing system overcomes pervasive off-target activity of direct fusion dCas9-DNMT3A constructs. Genome Res, 2018; 28:1193–1206. DOI: 10.1101/gr.233049.117.
103.
TanenbaumME, GilbertLA, QiLS, et al.A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell, 2014; 159:635–646. DOI: 10.1016/j.cell.2014.09.039.
104.
KonermannS, BrighamMD, TrevinoAE, et al.Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature, 2015; 517:583–588. DOI: 10.1038/nature14136.
LiZ, ZhangD, XiongX, et al.A potent Cas9-derived gene activator for plant and mammalian cells. Nat Plants, 2017; 3:930–936. DOI: 10.1038/s41477-017-0046-0.
107.
Cano-RodriguezD, GjaltemaRA, JilderdaLJ, et al.Writing of H3K4Me3 overcomes epigenetic silencing in a sustained but context-dependent manner. Nat Commun, 2016; 7:1228–4. DOI: 10.1038/ncomms12284.
108.
ChewWL, TabebordbarM, ChengJK, et al.A multifunctional AAV-CRISPR-Cas9 and its host response. Nat Methods, 2016; 13:868–874. DOI: 10.1038/nmeth.3993.
109.
MorenoAM, FuX, ZhuJ, et al.In situ gene therapy via AAV-CRISPR-Cas9-mediated targeted gene regulation. Mol Ther, 2018; 26:1818–1827. DOI: 10.1016/j.ymthe.2018.04.017.
110.
BraunSMG, KirklandJG, ChoryEJ, et al.Rapid and reversible epigenome editing by endogenous chromatin regulators. Nat Commun, 2017; 8:56–0. DOI: 10.1038/s41467-017-00644-y.
111.
LiszczakGP, BrownZZ, KimSH, et al.Genomic targeting of epigenetic probes using a chemically tailored Cas9 system. Proc Natl Acad Sci U S A, 2017; 114:681–686. DOI: 10.1073/pnas.1615723114.
112.
MorganSL, MarianoNC, BermudezA, et al.Manipulation of nuclear architecture through CRISPR-mediated chromosomal looping. Nat Commun, 2017; 8:1599–3. DOI: 10.1038/ncomms15993.
113.
HaoN, ShearwinKE, DoddIB. Programmable DNA looping using engineered bivalent dCas9 complexes. Nat Commun, 2017; 8:162–8. DOI: 10.1038/s41467-017-01873-x.
114.
MorganSL, ChangEY, MarianoNC, et al.CRISPR-mediated reorganization of chromatin loop structure. J Vis Exp, 2018. DOI: 10.3791/57457.
115.
JensenKT, FloeL, PetersenTS, et al.Chromatin accessibility and guide sequence secondary structure affect CRISPR-Cas9 gene editing efficiency. FEBS Lett, 2017; 591:1892–1901. DOI: 10.1002/1873-3468.12707.
116.
Uusi-MakelaMIE, BarkerHR, BauerleinCA, et al.Chromatin accessibility is associated with CRISPR-Cas9 efficiency in the zebrafish (Danio rerio). PLoS One, 2018; 13:e019623–8. DOI: 10.1371/journal.pone.0196238.
117.
ChenF, DingX, FengY, et al.Targeted activation of diverse CRISPR-Cas systems for mammalian genome editing via proximal CRISPR targeting. Nat Commun, 2017; 8:1495–8. DOI: 10.1038/ncomms14958.
118.
MaH, NaseriA, Reyes-GutierrezP, et al.Multicolor CRISPR labeling of chromosomal loci in human cells. Proc Natl Acad Sci U S A, 2015; 112:3002–3007. DOI: 10.1073/pnas.1420024112.
119.
ChenB, GilbertLA, CiminiBA, et al.Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 2013; 155:1479–1491. DOI: 10.1016/j.cell.2013.12.001.
120.
ChenB, HuJ, AlmeidaR, et al.Expanding the CRISPR imaging toolset with Staphylococcus aureus Cas9 for simultaneous imaging of multiple genomic loci. Nucl Acids Res, 2016; 44:e7–5. DOI: 10.1093/nar/gkv1533.
121.
FuY, RochaPP, LuoVM, et al.CRISPR-dCas9 and sgRNA scaffolds enable dual-colour live imaging of satellite sequences and repeat-enriched individual loci. Nat Commun, 2016; 7:1170–7. DOI: 10.1038/ncomms11707.
122.
MaassPG, BarutcuAR, WeinerCL, et al.Inter-chromosomal contact properties in live-cell imaging and in Hi-C. Mol Cell, 2018; 69:1039–1045. DOI: 10.1016/j.molcel.2018.02.007.
123.
WuX, MaoS, YangY, et al.A CRISPR/molecular beacon hybrid system for live-cell genomic imaging. Nucl Acids Res, 2018; 46:e8–0. DOI: 10.1093/nar/gky304.
124.
DengW, ShiX, TjianR, et al.CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proc Natl Acad Sci U S A, 2015; 112:11870–11875. DOI: 10.1073/pnas.1515692112.
125.
ZhouY, WangP, TianF, et al.Painting a specific chromosome with CRISPR/Cas9 for live-cell imaging. Cell Res, 2017; 27:298–301. DOI: 10.1038/cr.2017.9.
126.
NellesDA, FangMY, O'ConnellMR, et al.Programmable RNA tracking in live cells with CRISPR/Cas9. Cell, 2016; 165:488–496. DOI: 10.1016/j.cell.2016.02.054.
127.
AbudayyehOO, GootenbergJS, EssletzbichlerP, et al.RNA targeting with CRISPR-Cas13. Nature, 2017; 550:280–284. DOI: 10.1038/nature24049.
128.
ChoWK, JayanthN, MullenS, et al.Super-resolution imaging of fluorescently labeled, endogenous RNA polymerase II in living cells with CRISPR/Cas9-mediated gene editing. Sci Rep, 2016; 6:3594–9. DOI: 10.1038/srep35949.
129.
SavicD, PartridgeEC, NewberryKM, et al.CETCh-seq: CRISPR epitope tagging ChIP-seq of DNA-binding proteins. Genome Res, 2015; 25:1581–1589. DOI: 10.1101/gr.193540.115.
130.
SchmidtJC, ZaugAJ, CechTR. Live cell imaging reveals the dynamics of telomerase recruitment to telomeres. Cell, 2016; 166:1188–1197. DOI: 10.1016/j.cell.2016.07.033.
131.
CoxDBT, GootenbergJS, AbudayyehOO, et al.RNA editing with CRISPR-Cas13. Science, 2017; 358:1019–1027. DOI: 10.1126/science.aaq0180.
132.
BatraR, NellesDA, PirieE, et al.Elimination of toxic microsatellite repeat expansion RNA by RNA-targeting Cas9. Cell, 2017; 170:899–912. DOI: 10.1016/j.cell.2017.07.010.
133.
PintoBS, SaxenaT, OliveiraR, et al.Impeding transcription of expanded microsatellite repeats by deactivated Cas9. Mol Cell, 2017; 68:479–490. DOI: 10.1016/j.molcel.2017.09.033.
134.
KonermannS, LotfyP, BrideauNJ, et al.Transcriptome engineering with RNA-targeting type VI-D CRISPR effectors. Cell, 2018; 173:665–676. DOI: 10.1016/j.cell.2018.02.033.
135.
van AgtmaalEL, AndreLM, WillemseM, et al.CRISPR/Cas9-induced (CTGCAG)n repeat instability in the myotonic dystrophy type 1 locus: implications for therapeutic genome editing. Mol Ther, 2017; 25:24–43. DOI: 10.1016/j.ymthe.2016.10.014.
136.
ProvenzanoC, CappellaM, ValapertaR, et al.CRISPR/Cas9-mediated deletion of CTG expansions recovers normal phenotype in myogenic cells derived from myotonic dystrophy 1 patients. Mol Ther Nucl Acids, 2017; 9:337–348. DOI: 10.1016/j.omtn.2017.10.006.
137.
DastidarS, ArduiS, SinghK, et al.Efficient CRISPR/Cas9-mediated editing of trinucleotide repeat expansion in myotonic dystrophy patient-derived iPS and myogenic cells. Nucl Acids Res, 2018; 46:8275–8298. DOI: 10.1093/nar/gky548.
138.
JingX, XieB, ChenL, et al.Implementation of the CRISPR-Cas13a system in fission yeast and its repurposing for precise RNA editing. Nucl Acids Res, 2018; 46:e9–0. DOI: 10.1093/nar/gky433.
139.
ShechnerDM, HacisuleymanE, YoungerST, et al.Multiplexable, locus-specific targeting of long RNAs with CRISPR-Display. Nat Methods, 2015; 12:664–670. DOI: 10.1038/nmeth.3433.
140.
CliftD, McEwanWA, LabzinLI, et al.A method for the acute and rapid degradation of endogenous proteins. Cell, 2017; 171:1692–1706. DOI: 10.1016/j.cell.2017.10.033.
141.
NabetB, RobertsJM, BuckleyDL, et al.The dTAG system for immediate and target-specific protein degradation. Nat Chem Biol, 2018; 14:431–441. DOI: 10.1038/s41589-018-0021-8.
142.
MartinezV, LauritsenI, HobelT, et al.CRISPR/Cas9-based genome editing for simultaneous interference with gene expression and protein stability. Nucl Acids Res, 2017; 45:e17–1. DOI: 10.1093/nar/gkx797.
143.
EversB, JastrzebskiK, HeijmansJP, et al.CRISPR knockout screening outperforms shRNA and CRISPRi in identifying essential genes. Nat Biotechnol, 2016; 34:631–633. DOI: 10.1038/nbt.3536.
144.
Koike-YusaH, LiY, TanEP, et al.Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat Biotechnol, 2014; 32:267–273. DOI: 10.1038/nbt.2800.
145.
ZhouY, ZhuS, CaiC, et al.High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature, 2014; 509:487–491. DOI: 10.1038/nature13166.
146.
WangT, WeiJJ, SabatiniDM, et al.Genetic screens in human cells using the CRISPR-Cas9 system. Science, 2014; 343:80–84. DOI: 10.1126/science.1246981.
147.
LiW, XuH, XiaoT, et al.MAGeCK enables robust identification of essential genes from genome-scale CRISPR/Cas9 knockout screens. Genome Biol, 2014; 15:55–4. DOI: 10.1186/s13059-014-0554-4.
148.
SharonE, ChenSA, KhoslaNM, et al.Functional genetic variants revealed by massively parallel precise genome editing. Cell, 2018; 175:544–557. DOI: 10.1016/j.cell.2018.08.057.
149.
BianS, RepicM, GuoZ, et al.Genetically engineered cerebral organoids model brain tumor formation. Nat Methods, 2018; 15:631–639. DOI: 10.1038/s41592-018-0070-7.
150.
KlannTS, BlackJB, ChellappanM, et al.CRISPR-Cas9 epigenome editing enables high-throughput screening for functional regulatory elements in the human genome. Nat Biotechnol, 2017; 35:561–568. DOI: 10.1038/nbt.3853.
151.
GarstAD, BassaloMC, PinesG, et al.Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering. Nat Biotechnol, 2017; 35:48–55. DOI: 10.1038/nbt.3718.
152.
RajagopalN, SrinivasanS, KoosheshK, et al.High-throughput mapping of regulatory DNA. Nat Biotechnol, 2016; 34:167–174. DOI: 10.1038/nbt.3468.
153.
DaoLTM, Galindo-AlbarranAO, Castro-MondragonJA, et al.Genome-wide characterization of mammalian promoters with distal enhancer functions. Nat Genet, 2017; 49:1073–1081. DOI: 10.1038/ng.3884.
154.
LiuSJ, HorlbeckMA, ChoSW, et al.CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells. Science, 2017; 355. DOI: 10.1126/science.aah7111.
155.
ShenJP, ZhaoD, SasikR, et al.Combinatorial CRISPR-Cas9 screens for de novo mapping of genetic interactions. Nat Methods, 2017; 14:573–576. DOI: 10.1038/nmeth.4225.
156.
DuD, RoguevA, GordonDE, et al.Genetic interaction mapping in mammalian cells using CRISPR interference. Nat Methods, 2017; 14:577–580. DOI: 10.1038/nmeth.4286.
157.
HorlbeckMA, XuA, WangM, et al.Mapping the genetic landscape of human cells. Cell, 2018; 174:953–967. DOI: 10.1016/j.cell.2018.06.010.
158.
GalonskaC, CharltonJ, MatteiAL, et al.Genome-wide tracking of dCas9-methyltransferase footprints. Nat Commun, 2018; 9:59–7. DOI: 10.1038/s41467-017-02708-5.
159.
HannaRE, DoenchJG. A case of mistaken identity. Nat Biotechnol, 2018; 36:802–804. DOI: 10.1038/nbt.4208.
160.
MaY, ZhangJ, YinW, et al.Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat Methods, 2016; 13:1029–1035. DOI: 10.1038/nmeth.4027.
161.
HessGT, FresardL, HanK, et al.Directed evolution using dCas9-targeted somatic hypermutation in mammalian cells. Nat Methods, 2016; 13:1036–1042. DOI: 10.1038/nmeth.4038.
162.
HalperinSO, TouCJ, WongEB, et al.CRISPR-guided DNA polymerases enable diversification of all nucleotides in a tunable window. Nature, 2018; 560:248–252. DOI: 10.1038/s41586-018-0384-8.
163.
SadhuMJ, BloomJS, DayL, et al.CRISPR-directed mitotic recombination enables genetic mapping without crosses. Science, 2016; 352:1113–1116. DOI: 10.1126/science.aaf5124.
164.
SturmA, SaskoiE, TiborK, et al.Highly efficient RNAi and Cas9-based auto-cloning systems for C. elegans research. Nucl Acids Res, 2018; 46:e10–5. DOI: 10.1093/nar/gky516.
165.
GeisingerJM, TuranS, HernandezS, et al.In vivo blunt-end cloning through CRISPR/Cas9-facilitated non-homologous end-joining. Nucl Acids Res, 2016; 44:e7–6. DOI: 10.1093/nar/gkv1542.
166.
SheW, NiJ, ShuiK, et al.Rapid and error-free site-directed mutagenesis by a PCR-free in vitro CRISPR/Cas9-mediated mutagenic system. ACS Synth Biol, 2018; 7:2236–2244. DOI: 10.1021/acssynbio.8b00245.
167.
TangW, LiuDR. Rewritable multi-event analog recording in bacterial and mammalian cells. Science, 2018; 360. DOI: 10.1126/science.aap8992.
168.
ShethRU, YimSS, WuFL, et al.Multiplex recording of cellular events over time on CRISPR biological tape. Science, 2017; 358:1457–1461. DOI: 10.1126/science.aao0958.
169.
ShipmanSL, NivalaJ, MacklisJD, et al.Molecular recordings by directed CRISPR spacer acquisition. Science, 2016; 353:aaf117–5. DOI: 10.1126/science.aaf1175.
170.
PerliSD, CuiCH, LuTK. Continuous genetic recording with self-targeting CRISPR-Cas in human cells. Science, 2016; 353. DOI: 10.1126/science.aag0511.
171.
ShipmanSL, NivalaJ, MacklisJD, et al.CRISPR-Cas encoding of a digital movie into the genomes of a population of living bacteria. Nature, 2017; 547:345–349. DOI: 10.1038/nature23017.
172.
SchmidtF, CherepkovaMY, PlattRJ. Transcriptional recording by CRISPR spacer acquisition from RNA. Nature, 2018; 562:380–385. DOI: 10.1038/s41586-018-0569-1.
173.
FriedaKL, LintonJM, HormozS, et al.Synthetic recording and in situ readout of lineage information in single cells. Nature, 2017; 541:107–111. DOI: 10.1038/nature20777.
174.
RajB, WagnerDE, McKennaA, et al.Simultaneous single-cell profiling of lineages and cell types in the vertebrate brain. Nat Biotechnol, 2018; 36:442–450. DOI: 10.1038/nbt.4103.
175.
SpanjaardB, HuB, MiticN, et al.Simultaneous lineage tracing and cell-type identification using CRISPR-Cas9-induced genetic scars. Nat Biotechnol, 2018; 36:469–473. DOI: 10.1038/nbt.4124.
176.
MichlitsG, HubmannM, WuSH, et al.CRISPR-UMI: single-cell lineage tracing of pooled CRISPR-Cas9 screens. Nat Methods, 2017; 14:1191–1197. DOI: 10.1038/nmeth.4466.
177.
McKennaA, FindlayGM, GagnonJA, et al.Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science, 2016; 353:aaf790–7. DOI: 10.1126/science.aaf7907.
178.
KalhorR, KalhorK, MejiaL, et al.Developmental barcoding of whole mouse via homing CRISPR. Science, 2018; 361. DOI: 10.1126/science.aat9804.
179.
LiuY, ZhanY, ChenZ, et al.Directing cellular information flow via CRISPR signal conductors. Nat Methods, 2016; 13:938–944. DOI: 10.1038/nmeth.3994.
180.
LiuY, HanJ, ChenZ, et al.Engineering cell signaling using tunable CRISPR-Cpf1-based transcription factors. Nat Commun, 2017; 8:209–5. DOI: 10.1038/s41467-017-02265-x.
181.
KipnissNH, DingalP, AbbottTR, et al.Engineering cell sensing and responses using a GPCR-coupled CRISPR-Cas system. Nat Commun, 2017; 8:221–2. DOI: 10.1038/s41467-017-02075-1.
WeinbergBH, PhamNTH, CaraballoLD, et al.Large-scale design of robust genetic circuits with multiple inputs and outputs for mammalian cells. Nat Biotechnol, 2017; 35:453–462. DOI: 10.1038/nbt.3805.
184.
KianiS, BealJ, EbrahimkhaniMR, et al.CRISPR transcriptional repression devices and layered circuits in mammalian cells. Nat Methods, 2014; 11:723–726. DOI: 10.1038/nmeth.2969.
185.
ZalatanJG, LeeME, AlmeidaR, et al.Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell, 2015; 160:339–350. DOI: 10.1016/j.cell.2014.11.052.
186.
GanderMW, VranaJD, VojeWE, et al.Digital logic circuits in yeast with CRISPR-dCas9 NOR gates. Nat Commun, 2017; 8:1545–9. DOI: 10.1038/ncomms15459.
187.
Bondy-DenomyJ, GarciaB, StrumS, et al.Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins. Nature, 2015; 526:136–139. DOI: 10.1038/nature15254.
188.
Bondy-DenomyJ, PawlukA, MaxwellKL, et al.Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature, 2013; 493:429–432. DOI: 10.1038/nature11723.
189.
MaxwellKL, GarciaB, Bondy-DenomyJ, et al.The solution structure of an anti-CRISPR protein. Nat Commun, 2016; 7:1313–4. DOI: 10.1038/ncomms13134.
190.
Dong, GuoM, WangS, et al.Structural basis of CRISPR-SpyCas9 inhibition by an anti-CRISPR protein. Nature, 2017; 546:436–439. DOI: 10.1038/nature22377.
191.
ShinJ, JiangF, LiuJJ, et al.Disabling Cas9 by an anti-CRISPR DNA mimic. Sci Adv, 2017; 3:e170162–0. DOI: 10.1126/sciadv.1701620.
192.
HarringtonLB, DoxzenKW, MaE, et al.A broad-spectrum inhibitor of CRISPR-Cas9. Cell, 2017; 170:1224–1233.e15. DOI: 10.1016/j.cell.2017.07.037.
193.
HynesAP, RousseauGM, AgudeloD, et al.Widespread anti-CRISPR proteins in virulent bacteriophages inhibit a range of Cas9 proteins. Nat Commun, 2018; 9:291–9. DOI: 10.1038/s41467-018-05092-w.
194.
PawlukA, AmraniN, ZhangY, et al.Naturally occurring off-switches for CRISPR-Cas9. Cell, 2016; 167:1829–1838. DOI: 10.1016/j.cell.2016.11.017.
195.
RauchBJ, SilvisMR, HultquistJF, et al.Inhibition of CRISPR-Cas9 with bacteriophage proteins. Cell, 2017; 168:150–158. DOI: 10.1016/j.cell.2016.12.009.
196.
MarinoND, ZhangJY, BorgesAL, et al.Discovery of widespread type I and type V CRISPR-Cas inhibitors. Science, 2018; 362:240–242. DOI: 10.1126/science.aau5174.
197.
WattersKE, FellmannC, BaiHB, et al.Systematic discovery of natural CRISPR-Cas12a inhibitors. Science, 2018; 362:236–239. DOI: 10.1126/science.aau5138.
198.
PawlukA, StaalsRH, TaylorC, et al.Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat Microbiol, 2016; 1:1608–5. DOI: 10.1038/nmicrobiol.2016.85.
199.
LiJ, XuZ, ChupalovA, et al.Anti-CRISPR-based biosensors in the yeast S. cerevisiae. J Biol Eng, 2018; 12:1–1. DOI: 10.1186/s13036-018-0101-z.
200.
JiaC, HuaiC, DingJ, et al.New applications of CRISPR/Cas9 system on mutant DNA detection. Gene, 2018; 641:55–62. DOI: 10.1016/j.gene.2017.10.023.
201.
NachmansonD, LianS, SchmidtEK, et al.Targeted genome fragmentation with CRISPR/Cas9 enables fast and efficient enrichment of small genomic regions and ultra-accurate sequencing with low DNA input (CRISPR-DS). Genome Res, 2018; 28:1589–1599. DOI: 10.1101/gr.235291.118.
202.
QiuXY, ZhuLY, ZhuCS, et al.Highly effective and low-cost microRNA detection with CRISPR-Cas9. ACS Synth Biol, 2018; 7:807–813. DOI: 10.1021/acssynbio.7b00446.
203.
Bennett-BakerPE, MuellerJL. CRISPR-mediated isolation of specific megabase segments of genomic DNA. Nucl Acids Res, 2017; 45:e16–5. DOI: 10.1093/nar/gkx749.
204.
FujitaT, YunoM, FujiiH. Efficient sequence-specific isolation of DNA fragments and chromatin by in vitro enChIP technology using recombinant CRISPR ribonucleoproteins. Genes Cells, 2016; 21:370–377. DOI: 10.1111/gtc.12341.
205.
TsuiC, InouyeC, LevyM, et al.dCas9-targeted locus-specific protein isolation method identifies histone gene regulators. Proc Natl Acad Sci U S A, 2018; 115:E2734–E2741. DOI: 10.1073/pnas.1718844115.
206.
WaldripZJ, ByrumSD, StoreyAJ, et al.A CRISPR-based approach for proteomic analysis of a single genomic locus. Epigenetics, 2014; 9:1207–1211. DOI: 10.4161/epi.29919.
207.
FujitaT, FujiiH. Efficient isolation of specific genomic regions and identification of associated proteins by engineered DNA-binding molecule-mediated chromatin immunoprecipitation (enChIP) using CRISPR. Biochem Biophys Res Commun, 2013; 439:132–136. DOI: 10.1016/j.bbrc.2013.08.013.
208.
ZhanH, XieH, ZhouQ, et al.Synthesizing a genetic sensor based on CRISPR-Cas9 for specifically killing of P53-deficient cancer cells. ACS Synth Biol, 2018; 7:1798–1807. DOI: 10.1021/acssynbio.8b00202.
209.
LiuY, ZengY, LiuL, et al.Synthesizing AND gate genetic circuits based on CRISPR-Cas9 for identification of bladder cancer cells. Nat Commun, 2014; 5:539–3. DOI: 10.1038/ncomms6393.
210.
GootenbergJS, AbudayyehOO, KellnerMJ, et al.Multiplexed and portable nucleic acid detection platform with Cas13, Cas12a, and Csm6. Science, 2018; 360:439–444. DOI: 10.1126/science.aaq0179.
211.
GootenbergJS, AbudayyehOO, LeeJW, et al.Nucleic acid detection with CRISPR-Cas13a/C2c2. Science, 2017; 356:438–442. DOI: 10.1126/science.aam9321.
212.
MyhrvoldC, FreijeCA, GootenbergJS, et al.Field-deployable viral diagnostics using CRISPR-Cas13. Science, 2018; 360:444–448. DOI: 10.1126/science.aas8836.
213.
PardeeK, GreenAA, TakahashiMK, et al.Rapid, low-cost detection of Zika virus using programmable biomolecular components. Cell, 2016; 165:1255–1266. DOI: 10.1016/j.cell.2016.04.059.
214.
ZhangY, QianL, WeiW, et al.Paired design of dCas9 as a systematic platform for the detection of featured nucleic acid sequences in pathogenic strains. ACS Synth Biol, 2017; 6:211–216. DOI: 10.1021/acssynbio.6b00215.
215.
CaliendoAM, HodinkaRL. A CRISPR way to diagnose infectious diseases. N Engl J Med, 2017; 377:1685–1687. DOI: 10.1056/NEJMcibr1704902.
216.
WangQ, ZhangB, XuX, et al.CRISPR-typing PCR (ctPCR), a new Cas9-based DNA detection method. Sci Rep, 2018; 8:1412–6. DOI: 10.1038/s41598-018-32329-x.
217.
ChertowDS. Next-generation diagnostics with CRISPR. Science, 2018; 360:381–382. DOI: 10.1126/science.aat4982.
JuneCH, O'ConnorRS, KawalekarOU, et al.CAR T cell immunotherapy for human cancer. Science, 2018; 359:1361–1365. DOI: 10.1126/science.aar6711.
220.
RuppLJ, SchumannK, RoybalKT, et al.CRISPR/Cas9-mediated PD-1 disruption enhances anti-tumor efficacy of human chimeric antigen receptor T cells. Sci Rep, 2017; 7:73–7. DOI: 10.1038/s41598-017-00462-8.
221.
HuB, ZouY, ZhangL, et al.Nucleofection with plasmid DNA for CRISPR/Cas9-mediated inactivation of programmed cell death protein 1 in CD133-specific CAR T cells. Hum Gene Ther, 2018 Apr 27 [Epub ahead of print]. DOI: 10.1089/hum.2017.234.
222.
KimMY, YuKR, KenderianSS, et al.Genetic inactivation of CD33 in hematopoietic stem cells to enable CAR T cell immunotherapy for acute myeloid leukemia. Cell, 2018; 173:1439–1453. DOI: 10.1016/j.cell.2018.05.013.
223.
EyquemJ, Mansilla-SotoJ, GiavridisT, et al.Targeting a CAR to the TRAC locus with CRISPR/Cas9 enhances tumour rejection. Nature, 2017; 543:113–117. DOI: 10.1038/nature21405.
224.
ProvasiE, GenoveseP, LombardoA, et al.Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer. Nat Med, 2012; 18:807–815. DOI: 10.1038/nm.2700.
225.
TorikaiH, ReikA, LiuPQ, et al.A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR. Blood, 2012; 119:5697–5705. DOI: 10.1182/blood-2012-01-405365.
226.
WangJ, DeClercqJJ, HaywardSB, et al.Highly efficient homology-driven genome editing in human T cells by combining zinc-finger nuclease mRNA and AAV6 donor delivery. Nucl Acids Res, 2016; 44:e3–0. DOI: 10.1093/nar/gkv1121.
PoirotL, PhilipB, Schiffer-ManniouiC, et al.Multiplex genome-edited T-cell manufacturing platform for “off-the-shelf” adoptive T-cell immunotherapies. Cancer Res, 2015; 75:3853–3864. DOI: 10.1158/0008-5472.CAN-14-3321.
229.
MangusoRT, PopeHW, ZimmerMD, et al.In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target. Nature, 2017; 547:413–418. DOI: 10.1038/nature23270.
230.
HamptonT. Gene editing provides clues to why cancer immunotherapy often fails. JAMA, 2017; 318:1641–1642. DOI: 10.1001/jama.2017.15507.
231.
PatelSJ, SanjanaNE, KishtonRJ, et al.Identification of essential genes for cancer immunotherapy. Nature, 2017; 548:537–542. DOI: 10.1038/nature23477.
232.
PanD, KobayashiA, JiangP, et al.A major chromatin regulator determines resistance of tumor cells to T cell-mediated killing. Science, 2018; 359:770–775. DOI: 10.1126/science.aao1710.
TaoP, WuX, TangWC, et al.Engineering of bacteriophage T4 genome using CRISPR-Cas9. ACS Synth Biol, 2017; 6:1952–1961. DOI: 10.1021/acssynbio.7b00179.
235.
ShenJ, ZhouJ, ChenGQ, et al.Efficient genome engineering of a virulent Klebsiella bacteriophage using CRISPR-Cas9. J Virol, 2018; 92. DOI: 10.1128/JVI.00534-18.
236.
LinDM, KoskellaB, LinHC. Phage therapy: an alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol Ther, 2017; 8:162–173. DOI: 10.4292/wjgpt.v8.i3.162.
237.
BariSMN, WalkerFC, CaterK, et al.Strategies for editing virulent Staphylococcal phages using CRISPR-Cas10. ACS Synth Biol, 2017; 6:2316–2325. DOI: 10.1021/acssynbio.7b00240.
238.
HupfeldM, TrasanidouD, RamazziniL, et al.A functional type II-A CRISPR-Cas system from Listeria enables efficient genome editing of large non-integrating bacteriophage. Nucl Acids Res, 2018; 46:6920–6933. DOI: 10.1093/nar/gky544.
239.
de BuhrH, LebbinkRJ. Harnessing CRISPR to combat human viral infections. Curr Opin Immunol, 2018; 54:123–129. DOI: 10.1016/j.coi.2018.06.002.
240.
BarbuEM, CadyKC, HubbyB. Phage therapy in the era of synthetic biology. Cold Spring Harb Perspect Biol, 2016; 8. DOI: 10.1101/cshperspect.a023879.
241.
SenisE, FatourosC, GrosseS, et al.CRISPR/Cas9-mediated genome engineering: an adeno-associated viral (AAV) vector toolbox. Biotechnol J, 2014; 9:1402–1412. DOI: 10.1002/biot.201400046.
242.
MuzyczkaN, WarringtonKHJr. Custom adeno-associated virus capsids: the next generation of recombinant vectors with novel tropism. Hum Gene Ther, 2005; 16:408–416. DOI: 10.1089/hum.2005.16.408.
243.
LiangX, SunL, YuT, et al.A CRISPR/Cas9 and Cre/Lox system-based express vaccine development strategy against re-emerging Pseudorabies virus. Sci Rep, 2016; 6:1917–6. DOI: 10.1038/srep19176.
244.
MasonDM, WeberCR, ParolaC, et al.High-throughput antibody engineering in mammalian cells by CRISPR/Cas9-mediated homology-directed mutagenesis. Nucl Acids Res, 2018; 46:7436–7449. DOI: 10.1093/nar/gky550.
245.
KhoshnejadM, BrennerJS, MotleyW, et al.Molecular engineering of antibodies for site-specific covalent conjugation using CRISPR/Cas9. Sci Rep, 2018; 8:176–0. DOI: 10.1038/s41598-018-19784-2.
246.
PogsonM, ParolaC, KeltonWJ, et al.Immunogenomic engineering of a plug-and-(dis)play hybridoma platform. Nat Commun, 2016; 7:1253–5. DOI: 10.1038/ncomms12535.
247.
CheongTC, CompagnoM, ChiarleR. Editing of mouse and human immunoglobulin genes by CRISPR-Cas9 system. Nat Commun, 2016; 7:1093–4. DOI: 10.1038/ncomms10934.
248.
KeltonW, WaindokAC, PeschT, et al.Reprogramming MHC specificity by CRISPR-Cas9-assisted cassette exchange. Sci Rep, 2017; 7:4577–5. DOI: 10.1038/srep45775.
LeeHL, ShenH, HwangIY, et al.Targeted approaches for in situ gut microbiome manipulation. Genes (Basel), 2018; 9. DOI: 10.3390/genes9070351.
251.
RamG, RossHF, NovickRP, et al.Conversion of staphylococcal pathogenicity islands to CRISPR-carrying antibacterial agents that cure infections in mice. Nat Biotechnol, 2018; 36:971–976. DOI: 10.1038/nbt.4203.
252.
TakahashiK, YamanakaS. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 2006; 126:663–676. DOI: 10.1016/j.cell.2006.07.024.
253.
TakahashiK, TanabeK, OhnukiM, et al.Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 2007; 131:861–872. DOI: 10.1016/j.cell.2007.11.019.
254.
YuJ, VodyanikMA, Smuga-OttoK, et al.Induced pluripotent stem cell lines derived from human somatic cells. Science, 2007; 318:1917–1920. DOI: 10.1126/science.1151526.
255.
AmbasudhanR, TalantovaM, ColemanR, et al.Direct reprogramming of adult human fibroblasts to functional neurons under defined conditions. Cell Stem Cell, 2011; 9:113–118. DOI: 10.1016/j.stem.2011.07.002.
256.
ColasanteG, LignaniG, RubioA, et al.Rapid conversion of fibroblasts into functional forebrain GABAergic interneurons by direct genetic reprogramming. Cell Stem Cell, 2015; 17:719–734. DOI: 10.1016/j.stem.2015.09.002.
257.
HanDW, TapiaN, HermannA, et al.Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell, 2012; 10:465–472. DOI: 10.1016/j.stem.2012.02.021.
258.
HuangP, ZhangL, GaoY, et al.Direct reprogramming of human fibroblasts to functional and expandable hepatocytes. Cell Stem Cell, 2014; 14:370–384. DOI: 10.1016/j.stem.2014.01.003.
259.
IedaM, FuJD, Delgado-OlguinP, et al.Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell, 2010; 142:375–386. DOI: 10.1016/j.cell.2010.07.002.
260.
KaminskiMM, TosicJ, KresbachC, et al.Direct reprogramming of fibroblasts into renal tubular epithelial cells by defined transcription factors. Nat Cell Biol, 2016; 18:1269–1280. DOI: 10.1038/ncb3437.
261.
WapinskiOL, VierbuchenT, QuK, et al.Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell, 2013; 155:621–635. DOI: 10.1016/j.cell.2013.09.028.
262.
LiuP, ChenM, LiuY, et al.CRISPR-based chromatin remodeling of the endogenous Oct4 or Sox2 locus enables reprogramming to pluripotency. Cell Stem Cell, 2018; 22:252–261. DOI: 10.1016/j.stem.2017.12.001.
263.
WeltnerJ, BalboaD, KatayamaS, et al.Human pluripotent reprogramming with CRISPR activators. Nat Commun, 2018; 9:264–3. DOI: 10.1038/s41467-018-05067-x.
264.
NihongakiY, FuruhataY, OtabeT, et al.CRISPR-Cas9-based photoactivatable transcription systems to induce neuronal differentiation. Nat Methods, 2017; 14:963–966. DOI: 10.1038/nmeth.4430.
265.
BlackJB, AdlerAF, WangHG, et al.Targeted epigenetic remodeling of endogenous loci by CRISPR/Cas9-based transcriptional activators directly converts fibroblasts to neuronal cells. Cell Stem Cell, 2016; 19:406–414. DOI: 10.1016/j.stem.2016.07.001.
266.
ShaoJ, WangM, YuG, et al.Synthetic far-red light-mediated CRISPR-dCas9 device for inducing functional neuronal differentiation. Proc Natl Acad Sci U S A, 2018; 115:E6722–E6730. DOI: 10.1073/pnas.1802448115.
267.
IbraheimR, SongCQ, MirA, et al.All-in-one adeno-associated virus delivery and genome editing by Neisseria meningitidis Cas9 in vivo. Genome Biol, 2018; 19:13–7. DOI: 10.1186/s13059-018-1515-0.
268.
CharpentierM, KhedherAHY, MenoretS, et al.CtIP fusion to Cas9 enhances transgene integration by homology-dependent repair. Nat Commun, 2018; 9:113–3. DOI: 10.1038/s41467-018-03475-7.
269.
BasgallEM, GoettingSC, GoeckelME, et al.Gene drive inhibition by the anti-CRISPR proteins AcrIIA2 and AcrIIA4 in Saccharomyces cerevisiae. Microbiology, 2018; 164:464–474. DOI: 10.1099/mic.0.000635.
270.
ZhengY, ShenW, ZhangJ, et al.CRISPR interference-based specific and efficient gene inactivation in the brain. Nat Neurosci, 2018; 21:447–454. DOI: 10.1038/s41593-018-0077-5.
271.
CaliandoBJ, VoigtCA. Targeted DNA degradation using a CRISPR device stably carried in the host genome. Nat Commun, 2015; 6:698–9. DOI: 10.1038/ncomms7989.
272.
MoritaS, NoguchiH, HoriiT, et al.Targeted DNA demethylation in vivo using dCas9-peptide repeat and scFv-TET1 catalytic domain fusions. Nat Biotechnol, 2016; 34:1060-1065. DOI: 10.1038/nbt.3658.
273.
ZhouH, LiuJ, ZhouC, et al.In vivo simultaneous transcriptional activation of multiple genes in the brain using CRISPR-dCas9-activator transgenic mice. Nat Neurosci, 2018; 21:440–446. DOI: 10.1038/s41593-017-0060-6.
274.
NajmFJ, StrandC, DonovanKF, et al.Orthologous CRISPR-Cas9 enzymes for combinatorial genetic screens. Nat Biotechnol, 2018; 36:179–189. DOI: 10.1038/nbt.4048.
275.
KorkmazG, LopesR, UgaldeAP, et al.Functional genetic screens for enhancer elements in the human genome using CRISPR-Cas9. Nat Biotechnol, 2016; 34:192–198. DOI: 10.1038/nbt.3450.
276.
DatlingerP, RendeiroAF, SchmidlC, et al.Pooled CRISPR screening with single-cell transcriptome readout. Nat Methods, 2017; 14:297–301. DOI: 10.1038/nmeth.4177.
277.
BesterAC, LeeJD, ChavezA, et al.An integrated genome-wide CRISPRa approach to functionalize lncRNAs in drug resistance. Cell, 2018; 173:649–664.e20. DOI: 10.1016/j.cell.2018.03.052.
278.
ZimmermannM, MurinaO, ReijnsMAM, et al.CRISPR screens identify genomic ribonucleotides as a source of PARP-trapping lesions. Nature, 2018; 559:285–289. DOI: 10.1038/s41586-018-0291-z.
279.
O'ConnellMR, OakesBL, SternbergSH, et al.Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature, 2014; 516:263–266. DOI: 10.1038/nature13769.
NeguemborMV, Sebastian-PerezR, AulicinoF, et al.(Po)STAC (Polycistronic SunTAg modified CRISPR) enables live-cell and fixed-cell super-resolution imaging of multiple genes. Nucl Acids Res, 2018; 46:e3–0. DOI: 10.1093/nar/gkx1271.
282.
QinP, ParlakM, KuscuC, et al.Live cell imaging of low- and non-repetitive chromosome loci using CRISPR-Cas9. Nat Commun, 2017; 8:1472–5. DOI: 10.1038/ncomms14725.
283.
LiuX, ZhangY, ChenY, et al.In situ capture of chromatin interactions by biotinylated dCas9. Cell, 2017; 170:1028–1043. DOI: 10.1016/j.cell.2017.08.003.
284.
ZhangS, VoigtCA. Engineered dCas9 with reduced toxicity in bacteria: implications for genetic circuit design. Nucl Acids Res, 2018; 46:11115–11125. DOI: 10.1093/nar/gky884.
285.
TarasavaK, LiuR, GarstA, et al.Combinatorial pathway engineering using type I-E CRISPR interference. Biotechnol Bioeng, 2018; 115:1878–1883. DOI: 10.1002/bit.26589.
286.
WuMY, SungLY, LiH, et al.Combining CRISPR and CRISPRi systems for metabolic engineering of E. coli and 1,4-BDO biosynthesis. ACS Synth Biol, 2017; 6:2350–2361. DOI: 10.1021/acssynbio.7b00251.
287.
ShenCC, SungLY, LinSY, et al.Enhancing protein production yield from Chinese hamster ovary cells by CRISPR interference. ACS Synth Biol, 2017; 6:1509–1519. DOI: 10.1021/acssynbio.7b00020.
288.
MikuniT, NishiyamaJ, SunY, et al.High-throughput, high-resolution mapping of protein localization in mammalian brain by in vivo genome editing. Cell, 2016; 165:1803–1817. DOI: 10.1016/j.cell.2016.04.044.
289.
LeonettiMD, SekineS, KamiyamaD, et al.A scalable strategy for high-throughput GFP tagging of endogenous human proteins. Proc Natl Acad Sci U S A, 2016; 113:E3501–3508. DOI: 10.1073/pnas.1606731113.
290.
MyersSA, WrightJ, PecknerR, et al.Discovery of proteins associated with a predefined genomic locus via dCas9-APEX-mediated proximity labeling. Nat Methods, 2018; 15:437–439. DOI: 10.1038/s41592-018-0007-1.
291.
UemuraT, MoriT, KuriharaT, et al.Fluorescent protein tagging of endogenous protein in brain neurons using CRISPR/Cas9-mediated knock-in and in utero electroporation techniques. Sci Rep, 2016; 6:3586–1. DOI: 10.1038/srep35861.
292.
KorthoutT, Poramba-LiyanageDW, van KruijsbergenI, et al.Decoding the chromatin proteome of a single genomic locus by DNA sequencing. PLoS Biol, 2018; 16:e200554–2. DOI: 10.1371/journal.pbio.2005542.
293.
MikheikinA, OlsenA, LeslieK, et al.DNA nanomapping using CRISPR-Cas9 as a programmable nanoparticle. Nat Commun, 2017; 8:166–5. DOI: 10.1038/s41467-017-01891-9.
294.
ZhangB, XiaQ, WangQ, et al.Detecting and typing target DNA with a novel CRISPR-typing PCR (ctPCR) technique. Anal Biochem, 2018; 561–562:37–46. DOI: 10.1016/j.ab.2018.09.012.
295.
WeiS, ZouQ, LaiS, et al.Conversion of embryonic stem cells into extraembryonic lineages by CRISPR-mediated activators. Sci Rep, 2016; 6:1964–8. DOI: 10.1038/srep19648.
296.
LeeJ, LimH, JangH, et al.CRISPR-Cap: multiplexed double-stranded DNA enrichment based on the CRISPR system. Nucl Acids Res, 2018. DOI: 10.1093/nar/gky820.
297.
RothTL, Puig-SausC, YuR, et al.Reprogramming human T cell function and specificity with non-viral genome targeting. Nature, 2018; 559:405–409. DOI: 10.1038/s41586-018-0326-5.
298.
ReinshagenC, BhereD, ChoiSH, et al.CRISPR-enhanced engineering of therapy-sensitive cancer cells for self-targeting of primary and metastatic tumors. Sci Transl Med, 2018;10. DOI: 10.1126/scitranslmed.aao3240.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
