Browse > Article
http://dx.doi.org/10.4014/jmb.1607.07005

The CRISPR Growth Spurt: from Bench to Clinic on Versatile Small RNAs  

Bayat, Hadi (Medical Nano-Technology & Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences)
Omidi, Meysam (Medical Nano-Technology & Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences)
Rajabibazl, Masoumeh (Department of Clinical Biochemistry, School of Medicine, Shahid Beheshti University of Medical Sciences)
Sabri, Suriana (Department of Microbiology, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia)
Rahimpour, Azam (Medical Nano-Technology & Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences)
Publication Information
Journal of Microbiology and Biotechnology / v.27, no.2, 2017 , pp. 207-218 More about this Journal
Abstract
Clustered regulatory interspaced short palindromic repeats (CRISPR) in association with CRISPR-associated protein (Cas) is an adaptive immune system, playing a pivotal role in the defense of bacteria and archaea. Ease of handling and cost effectiveness make the CRISPR-Cas system an ideal programmable nuclease tool. Recent advances in understanding the CRISPR-Cas system have tremendously improved its efficiency. For instance, it is possible to recapitulate the chronicle CRISPR-Cas from its infancy and inaugurate a developed version by generating novel variants of Cas proteins, subduing off-target effects, and optimizing of innovative strategies. In summary, the CRISPR-Cas system could be employed in a number of applications, including providing model systems, rectification of detrimental mutations, and antiviral therapies.
Keywords
CRISPR-Cas system; DNA repair; adoptive immunity; genome editing;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Choi KY, Silvestre OF, Huang X, Hida N, Liu G, Ho DN, et al. 2014. A nanoparticle formula for delivering siRNA or miRNAs to tumor cells in cell culture and in vivo. Nat. Protoc. 9: 1900-1915.   DOI
2 Pattanayak V, Lin S, Guilinger JP, Ma E, Doudna JA, Liu DR. 2013. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31: 839-843.   DOI
3 Li L, He ZY, Wei XW, Gao GP, Wei YQ. 2015. Challenges in CRISPR/Cas9 delivery: potential roles of nonviral vectors. Hum. Gene Ther. 26: 452-462.   DOI
4 Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS, Kriz AJ, et al. 2015. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520: 186-191.   DOI
5 Kotterman MA, Schaffer DV. 2014. Engineering adenoassociated viruses for clinical gene therapy. Nat. Rev. Genet. 15: 445-451.   DOI
6 Sun W, Ji W, Hall JM, Hu Q, Wang C, Beisel CL, Gu Z. 2015. Self-assembled DNA nanoclews for the efficient delivery of CRISPR-Cas9 for genome editing. Angew. Chem. Int. Ed. Engl. 54: 12029-12033.   DOI
7 Sharei A, Zoldan J, Adamo A, Sim WY, Cho N, Jackson E, et al. 2013. A vector-free microfluidic platform for intracellular delivery. Proc. Natl. Acad. Sci. USA 110: 2082-2087.   DOI
8 Han X, Liu Z, Jo MC, Zhang K, Li Y, Zeng Z, et al. 2015. CRISPR-Cas9 delivery to hard-to-transfect cells via membrane deformation. Sci. Adv. 1: e1500454.   DOI
9 Wang L, Li F, Dang L, Liang C, Wang C, He B, et al. 2016. In vivo delivery systems for therapeutic genome editing. Int. J. Mol. Sci. 17: pii: E626.   DOI
10 Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR. 2016. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533: 420-424.   DOI
11 Zhang Y, Ge X, Yang F, Zhang L, Zheng J, Tan X, et al. 2014. Comparison of non-canonical PAMs for CRISPR/Cas9- mediated DNA cleavage in human cells. Sci. Rep. 4: 5405.
12 Jiang F, Zhou K, Ma L, Gressel S, Doudna JA. 2015. Structural biology. A Cas9-guide RNA complex preorganized for target DNA recognition. Science 348: 1477-1481.   DOI
13 Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, Cox DB, et al. 2016. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353: aaf5573.   DOI
14 Sternberg SH, LaFrance B, Kaplan M, Doudna JA. 2015. Conformational control of DNA target cleavage by CRISPRCas9. Nature 527: 110-113.   DOI
15 O'Connell MR, Oakes BL, Sternberg SH, East-Seletsky A, Kaplan M, Doudna JA. 2014. Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516: 263-266.   DOI
16 Silas S, Mohr G, Sidote DJ, Markham LM, Sanchez-Amat A, Bhaya D, et al. 2016. Direct CRISPR spacer acquisition from RNA by a natural reverse transcriptase-Cas1 fusion protein. Science 351: aad4234.   DOI
17 Shen B, Zhang W, Zhang J, Zhou J, Wang J, Chen L, et al. 2014. Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat. Methods 11: 399-402.   DOI
18 Ma H, Tu LC, Naseri A, Huisman M, Zhang S, Grunwald D, Pederson T. 2016. Multiplexed labeling of genomic loci with d Cas9 a nd engineered sgRNAs u sing CRISPRainbow. Nat. Biotechnol. 34: 528-530.   DOI
19 Mandegar MA, Huebsch N, Frolov EB, Shin E, Truong A, Olvera MP, et al. 2016. CRISPR interference efficiently induces specific and reversible gene silencing in human iPSCs. 18: 1-13.   DOI
20 Kiani S, Chavez A, Tuttle M, Hall RN, Chari R, Ter-Ovanesyan D, et al. 2015. Cas9 gRNA engineering for genome editing, activation and repression. Nat. Methods 12: 1051-1054.   DOI
21 Nakamura K, Fujii W, Tsuboi M, Tanihata J, Teramoto N, Takeuchi S, et al. 2014. Generation of muscular dystrophy model rats with a CRISPR/Cas system. Sci. Rep. 4: 5635.
22 Mao XY, Dai JX, Zhou HH, Liu ZQ, Jin WL. 2016. Brain tumor modeling using the CRISPR/Cas9 system: state of the art and view to the future. Oncotarget 7: 33461-33471.   DOI
23 Matano M, Date S, Shimokawa M, Takano A, Fujii M, Ohta Y, et al. 2015. Modeling colorectal cancer using CRISPRCas9- mediated engineering of human intestinal organoids. Nat. Med. 21: 256-262.   DOI
24 Bosze Z, Major P, Baczko I, Odening KE, Bodrogi L, Hiripi L, Varro A. 2016. The potential impact of new generation transgenic methods on creating rabbit models of cardiac diseases. Prog. Biophys. Mol. Biol. 121: 123-130.   DOI
25 Dow LE. 2015. Modeling disease in vivo with CRISPR/Cas9. Trends Mol. Med. 21: 609-621.   DOI
26 Kato T, Takada S. 2016. In vivo and in vitro disease modeling with CRISPR/Cas9. Brief. Funct. Genomics pii: elw031.
27 Kraft K, Geuer S, Will AJ, Chan WL, Paliou C, Borschiwer M, et al. 2015. Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice. Cell Rep. pii: S2211-S1247.
28 Dow LE, Fisher J, O'Rourke KP, Muley A, Kastenhuber ER, Livshits G, et al. 2015. Inducible in vivo genome editing with CRISPR-Cas9. Nat. Biotechnol. 33: 390-394.   DOI
29 Black JB, Adler AF, Wang H-G, D'Ippolito AM, Hutchinson HA, Reddy TE, et al. 2016. Targeted epigenetic remodeling of endogenous loci by CRISPR/Cas9-based transcriptional activators directly converts fibroblasts to neuronal cells. Cell Stem Cell 19: 1-9.   DOI
30 Thakore PI, Black JB, Hilton IB, Gersbach CA. 2016. Editing the epigenome: technologies for programmable transcription and epigenetic modulation. Nat. Methods 13: 127-137.   DOI
31 Kim D, Bae S, Park J, Kim E, Kim S, Yu HR, et al. 2015. Digenome-seq: genome-wide profiling of CRISPR-Cas9 offtarget effects in human cells. Nat. Methods 12: 237-243, 1 p. following 243.   DOI
32 Lin S, Staahl BT, Alla RK, Doudna JA. 2014. Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. Elife 3: e04766.
33 Howden SE, McColl B, Glaser A, Vadolas J, Petrou S, Little MH, et al. 2016. A Cas9 variant for efficient generation of indel-free knockin or gene-corrected human pluripotent stem cells. Stem. Cell Reports 7: 508-517.   DOI
34 Carroll D. 2014. Genome engineering with targetable nucleases. Annu. Rev. Biochem. 83: 409-439.   DOI
35 Fonfara I, Richter H, Bratovic M, Le Rhun A, Charpentier E. 2016. The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature 532: 517-521.   DOI
36 Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13: 722-736.   DOI
37 Chylinski K, Le Rhun A, Charpentier E. 2013. The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 10: 726-737.   DOI
38 Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, et al. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163: 759-771.   DOI
39 Tsai SQ, Joung JK. 2016. Defining and improving the genome-wide specificities of CRISPR-Cas9 nucleases. Nat. Rev. Genet. 17: 300-312.   DOI
40 Cong L, Ran F, Cox D, Lin S, Barretto R, Habib N, et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 5.
41 Wang T, Wei JJ, Sabatini DM, Lander ES. 2014. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343: 80-84.   DOI
42 Kuscu C, Arslan S, Singh R, Thorpe J, Adli M. 2014. Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat. Biotechnol. 32: 677-683.   DOI
43 Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPRCas systems. Nat. Biotechnol. 31: 233-242.   DOI
44 Doench JG, Hartenian E, Graham DB, Tothova Z, Hegde M, Smith I, et al. 2014. Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol. 32: 1262-1267.   DOI
45 Wyvekens N, Topkar VV, Khayter C, Joung JK, Tsai SQ. 2015. Dimeric CRISPR RNA-guided FokI-dCas9 nucleases directed by truncated gRNAs for highly specific genome editing. Hum. Gene Ther. 26: 425-431.   DOI
46 Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8: 28.
47 Frock RL, Hu J, Meyers RM, Ho YJ, Kii E, Alt FW. 2015. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat. Biotechnol. 33: 179-186.   DOI
48 Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, et al. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389.   DOI
49 Guilinger JP, Thompson DB, Liu DR. 2014. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat. Biotechnol. 32: 577-582.   DOI
50 Hara S, Tamano M, Yamashita S, Kato T, Saito T, Sakuma T, et al. 2015. Generation of mutant mice via the CRISPR/Cas9 system using FokI-dCas9. Sci. Rep. 5: 11221.   DOI
51 Tabebordbar M, Zhu K, Cheng JK, Chew WL, Widrick JJ, Yan WX, et al. 2015. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 531: 407-411.
52 Banan M, Bayat H, Azarkeivan A, Mohammadparast S, Kamali K, Farashi S, et al. 2012. The XmnI and BCL11A single nucleotide polymorphisms may help predict hydroxyurea response in Iranian beta-thalassemia patients. Hemoglobin 36: 371-380.   DOI
53 Banan M, Bayat H, Namdar-Aligoodarzi P, Azarkeivan A, Kamali K, Daneshmand P, et al. 2013. Utility of the multivariate approach in predicting beta-thalassemia intermedia or betathalassemia major types In Iranian patients. Hemoglobin 37: 413-422.   DOI
54 Bauer DE, Kamran SC, Lessard S, Xu J, Fujiwara Y, Lin C, et al. 2013. An erythroid enhancer of BCL11A subject to genetic variation determines fetal hemoglobin level. Science 342: 253-257.   DOI
55 Courtney DG, Moore JE, Atkinson SD, Maurizi E, Allen EH, Pedrioli DM, et al. 2016. CRISPR/Cas9 DNA cleavage at SNP-derived PAM enables both in vitro and in vivo KRT12 mutation-specific targeting. Gene Ther. 23: 108-112.   DOI
56 Taylor DW, Zhu Y, Staals RH, Kornfeld JE, Shinkai A, van der Oost J, et al. 2015. Structural biology. Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning. Science 348: 581-585.   DOI
57 Jamal M, Khan FA, Da L, Habib Z, Dai J, Cao G. 2015. Keeping CRISPR/Cas on-target. Curr. Issues Mol. Biol. 20: 1-20.
58 Kennedy EM, Cullen BR. 2015. Bacterial CRISPR/Cas DNA endonucleases: a revolutionary technology that could dramatically impact viral research and treatment. Virology 479-480: 213-220.   DOI
59 Rahimpour A, Ahani R, Najaei A, Adeli A, Barkhordari F, Mahboudi F. 2016. Development of genetically modified Chinese hamster ovary host cells for the enhancement of recombinant tissue plasminogen activator expression. Malays. J. Med. Sci. 23: 6-13.
60 Lee JS, Grav LM, Lewis NE, Faustrup Kildegaard H. 2015. CRISPR/Cas9-mediated genome engineering of CHO cell factories: application and perspectives. Biotechnol. J. 10: 979-994.   DOI
61 Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng Z, et al. 2015. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523: 481-485.   DOI
62 Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32: 279-284.   DOI
63 Savic N, Schwank G. 2016. Advances in therapeutic CRISPR/Cas9 genome editing. Transl. Res. 168: 15-21.   DOI
64 Reardon S. 2016. First CRISPR clinical trial gets green light from US panel. Nature News. Available at http://www.nature.com/news/first-crispr-clinical-trial-gets-greenlight- from-us-panel-1.20137.
65 Richardson CD, Ray GJ, DeWitt MA, Curie GL, Corn JE. 2016. Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat. Biotechnol. 34: 339-344.   DOI
66 Baltimore D, Berg P, Botchan M, Carroll D, Charo RA, Church G, et al. 2015. Biotechnology. A prudent path forward for genomic engineering and germline gene modification. Science 348: 36-38.   DOI
67 Gao Y, Zhao Y. 2014. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPRmediated genome editing. J. Integr. Plant Biol. 56: 343-349.   DOI
68 Morrical SW. 2015. DNA-pairing and annealing processes in homologous recombination and homology-directed repair. Cold Spring Harb. Perspect. Biol. 7: a016444.   DOI
69 Hendel A, Bak RO, Clark JT, Kennedy AB, Ryan DE, Roy S, et al. 2015. Chemically modified guide RNAs enhance CRISPR-Cas genome editing in human primary cells. Nat. Biotechnol. 33: 985-989.   DOI
70 Liang X, Potter J, Kumar S, Zou Y, Quintanilla R, Sridharan M, et al. 2015. Rapid and highly efficient mammalian cell engineering via Cas9 protein transfection. J. Biotechnol. 208: 44-53.   DOI
71 Maruyama T, Dougan SK, Truttmann MC, Bilate AM, Ingram JR, Ploegh HL. 2015. Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol. 33: 538-542.   DOI
72 Song J, Yang D, Xu J, Zhu T, Chen YE, Zhang J. 2016. RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency. Nat. Commun. 7: 10548.   DOI
73 Chu VT, Weber T, Wefers B, Wurst W, Sander S, Rajewsky K, Kuhn R. 2015. Increasing the efficiency of homologydirected repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat. Biotechnol. 33: 543-548.   DOI
74 Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Joung JK. 2016. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529: 490-495.   DOI
75 Bolukbasi MF, Gupta A, Oikemus S, Derr AG, Garber M, Brodsky MH, et al. 2015. DNA-binding-domain fusions enhance the targeting range and precision of Cas9. Nat. Methods 12: 1150-1156.   DOI
76 Wright AV, Sternberg SH, Taylor DW, Staahl BT, Bardales JA, Kornfeld JE, Doudna JA. 2015. Rational design of a split-Cas9 enzyme complex. Proc. Natl. Acad. Sci. USA 112: 2984-2989.   DOI
77 Polstein LR, Gersbach CA. 2015. A light-inducible CRISPRCas9 system for control of endogenous gene activation. Nat. Chem. Biol. 11: 198-200.   DOI
78 Zetsche B, Volz SE, Zhang F. 2015. A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat. Biotechnol. 33: 139-142.   DOI
79 Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. 2016. Rationally engineered Cas9 nucleases with improved specificity. Science 351: 84-88.   DOI
80 Anders C, Niewoehner O, Duerst A, Jinek M. 2014. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513: 569-573.   DOI
81 Jinek M, Jiang F, Taylor DW, Sternberg SH, Kaya E, Ma E, et al. 2014. Structures of Cas9 endonucleases reveal RNAmediated conformational activation. Science 343: 1247997.   DOI
82 Tsai SQ, Zheng Z, Nguyen NT, Liebers M, Topkar VV, Thapar V, et al. 2015. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat. Biotechnol. 33: 187-197.   DOI
83 Mohammadparast S, Bayat H, Biglarian A, Ohadi M. 2014. Exceptional expansion and conservation of a CT-repeat complex in the core promoter of PAXBP1 in primates. Am. J. Primatol. 76: 747-756.   DOI
84 Sontheimer EJ, Marraffini LA. 2016. RNA. CRISPR goes retro. Science 351: 920-921.   DOI
85 Kopfmann S, Hess WR. 2013. Toxin-antitoxin systems on the large defense plasmid pSYSA of Synechocystis sp. PCC 6803. J. Biol. Chem. 288: 7399-7409.   DOI
86 Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821.   DOI
87 Levasseur A, Bekliz M, Chabriere E, Pontarotti P, La Scola B, Raoult D. 2016. MIMIVIRE is a defence system in mimivirus that confers resistance to virophage. Nature 531: 249-252.   DOI
88 Lander ES. 2016. The heroes of CRISPR. Cell 164: 18-28.   DOI
89 Jansen R, Embden J, Gaastra W, Schouls L. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43: 10.
90 Makarova KS, Koonin EV. 2015. Annotation and classification of CRISPR-Cas systems. Methods Mol. Biol. 1311: 47-75.
91 Mei Y, Wang Y, Chen H, Sun ZS, Ju XD. 2016. Recent progress in CRISPR/Cas9 technology. J. Genet. Genomics 43: 63-75.   DOI
92 Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170.   DOI
93 Doudna JA, Charpentier E. 2014. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346: 1258096.   DOI
94 Mohanraju P, Makarova KS, Zetsche B, Zhang F, Koonin EV, van der Oost J. 2016. Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353: aad5147.   DOI
95 Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, et al. 2011. CRISPR RNA maturation by transencod ed small RNA a nd host factor RNase III. Nature 471: 602-607.   DOI
96 Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA. 2014. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507: 62-67.   DOI