DOI QR코드

DOI QR Code

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)
  • Received : 2016.07.04
  • Accepted : 2016.11.12
  • Published : 2017.02.28

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

References

  1. 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. https://doi.org/10.1074/jbc.M112.434100
  2. 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. https://doi.org/10.1126/science.1225829
  3. 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. https://doi.org/10.1038/nature17146
  4. Lander ES. 2016. The heroes of CRISPR. Cell 164: 18-28. https://doi.org/10.1016/j.cell.2015.12.041
  5. Jansen R, Embden J, Gaastra W, Schouls L. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43: 10.
  6. Sontheimer EJ, Marraffini LA. 2016. RNA. CRISPR goes retro. Science 351: 920-921. https://doi.org/10.1126/science.aaf2851
  7. Makarova KS, Koonin EV. 2015. Annotation and classification of CRISPR-Cas systems. Methods Mol. Biol. 1311: 47-75.
  8. Mei Y, Wang Y, Chen H, Sun ZS, Ju XD. 2016. Recent progress in CRISPR/Cas9 technology. J. Genet. Genomics 43: 63-75. https://doi.org/10.1016/j.jgg.2016.01.001
  9. Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170. https://doi.org/10.1126/science.1179555
  10. Doudna JA, Charpentier E. 2014. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346: 1258096. https://doi.org/10.1126/science.1258096
  11. 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. https://doi.org/10.1126/science.aad5147
  12. 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. https://doi.org/10.1038/nature09886
  13. Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA. 2014. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507: 62-67. https://doi.org/10.1038/nature13011
  14. 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.
  15. 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. https://doi.org/10.1126/science.aab1452
  16. Sternberg SH, LaFrance B, Kaplan M, Doudna JA. 2015. Conformational control of DNA target cleavage by CRISPRCas9. Nature 527: 110-113. https://doi.org/10.1038/nature15544
  17. 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. https://doi.org/10.1038/nature13769
  18. 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. https://doi.org/10.1126/science.aad4234
  19. 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. https://doi.org/10.1126/science.aaf5573
  20. 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. https://doi.org/10.1038/nmeth.2857
  21. 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. https://doi.org/10.1038/nbt.3526
  22. 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. https://doi.org/10.1016/j.stem.2015.12.009
  23. 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. https://doi.org/10.1038/nmeth.3580
  24. 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. https://doi.org/10.1038/nrmicro3569
  25. 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. https://doi.org/10.4161/rna.24321
  26. 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. https://doi.org/10.1016/j.cell.2015.09.038
  27. 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. https://doi.org/10.1038/nature17945
  28. Tsai SQ, Joung JK. 2016. Defining and improving the genome-wide specificities of CRISPR-Cas9 nucleases. Nat. Rev. Genet. 17: 300-312. https://doi.org/10.1038/nrg.2016.28
  29. 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.
  30. Wang T, Wei JJ, Sabatini DM, Lander ES. 2014. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343: 80-84. https://doi.org/10.1126/science.1246981
  31. 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. https://doi.org/10.1038/nbt.2916
  32. 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. https://doi.org/10.1038/nbt.2508
  33. 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. https://doi.org/10.1038/nbt.3026
  34. 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.
  35. 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. https://doi.org/10.1126/science.aaa4535
  36. 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. https://doi.org/10.1038/nature14592
  37. 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. https://doi.org/10.1038/nbt.2808
  38. 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. https://doi.org/10.1038/nbt.3290
  39. 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. https://doi.org/10.1016/j.jbiotec.2015.04.024
  40. Morrical SW. 2015. DNA-pairing and annealing processes in homologous recombination and homology-directed repair. Cold Spring Harb. Perspect. Biol. 7: a016444. https://doi.org/10.1101/cshperspect.a016444
  41. 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. https://doi.org/10.1038/nbt.3190
  42. 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. https://doi.org/10.1038/ncomms10548
  43. 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. https://doi.org/10.1038/nbt.3198
  44. 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.
  45. 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. https://doi.org/10.1016/j.stemcr.2016.07.001
  46. Carroll D. 2014. Genome engineering with targetable nucleases. Annu. Rev. Biochem. 83: 409-439. https://doi.org/10.1146/annurev-biochem-060713-035418
  47. 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. https://doi.org/10.1038/nmeth.3284
  48. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8: 28.
  49. 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. https://doi.org/10.1038/nbt.3101
  50. 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. https://doi.org/10.1016/j.cell.2013.08.021
  51. 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. https://doi.org/10.1089/hum.2015.084
  52. 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. https://doi.org/10.1038/nbt.2909
  53. 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. https://doi.org/10.1038/srep11221
  54. 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. https://doi.org/10.1038/nmeth.3624
  55. 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. https://doi.org/10.1073/pnas.1501698112
  56. Polstein LR, Gersbach CA. 2015. A light-inducible CRISPRCas9 system for control of endogenous gene activation. Nat. Chem. Biol. 11: 198-200. https://doi.org/10.1038/nchembio.1753
  57. Zetsche B, Volz SE, Zhang F. 2015. A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat. Biotechnol. 33: 139-142. https://doi.org/10.1038/nbt.3149
  58. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. 2016. Rationally engineered Cas9 nucleases with improved specificity. Science 351: 84-88. https://doi.org/10.1126/science.aad5227
  59. 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. https://doi.org/10.1038/nature16526
  60. 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. https://doi.org/10.1038/nature13579
  61. 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. https://doi.org/10.1126/science.1247997
  62. 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. https://doi.org/10.1038/nbt.3117
  63. 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. https://doi.org/10.1002/ajp.22266
  64. 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. https://doi.org/10.1038/nprot.2014.128
  65. 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. https://doi.org/10.1038/nbt.2673
  66. 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. https://doi.org/10.1089/hum.2015.069
  67. 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. https://doi.org/10.1038/nature14299
  68. Kotterman MA, Schaffer DV. 2014. Engineering adenoassociated viruses for clinical gene therapy. Nat. Rev. Genet. 15: 445-451. https://doi.org/10.1038/nrg3742
  69. 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. https://doi.org/10.1002/anie.201506030
  70. 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. https://doi.org/10.1073/pnas.1218705110
  71. 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. https://doi.org/10.1126/sciadv.1500454
  72. 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. https://doi.org/10.3390/ijms17050626
  73. 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. https://doi.org/10.1038/nature17946
  74. 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. https://doi.org/10.18632/oncotarget.8075
  75. 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. https://doi.org/10.1038/nm.3802
  76. 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. https://doi.org/10.1016/j.pbiomolbio.2016.05.007
  77. 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.
  78. Dow LE. 2015. Modeling disease in vivo with CRISPR/Cas9. Trends Mol. Med. 21: 609-621. https://doi.org/10.1016/j.molmed.2015.07.006
  79. Kato T, Takada S. 2016. In vivo and in vitro disease modeling with CRISPR/Cas9. Brief. Funct. Genomics pii: elw031.
  80. 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.
  81. 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. https://doi.org/10.1038/nbt.3155
  82. Thakore PI, Black JB, Hilton IB, Gersbach CA. 2016. Editing the epigenome: technologies for programmable transcription and epigenetic modulation. Nat. Methods 13: 127-137. https://doi.org/10.1038/nmeth.3733
  83. 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. https://doi.org/10.1016/j.stem.2016.06.014
  84. 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. https://doi.org/10.3109/03630269.2012.691147
  85. 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. https://doi.org/10.3109/03630269.2013.805418
  86. 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. https://doi.org/10.1126/science.1242088
  87. 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.
  88. 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. https://doi.org/10.1038/gt.2015.82
  89. 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. https://doi.org/10.1016/j.virol.2015.02.024
  90. 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.
  91. 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. https://doi.org/10.1002/biot.201500082
  92. 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.
  93. 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. https://doi.org/10.1038/nbt.3481
  94. 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. https://doi.org/10.1126/science.aab1028
  95. Savic N, Schwank G. 2016. Advances in therapeutic CRISPR/Cas9 genome editing. Transl. Res. 168: 15-21. https://doi.org/10.1016/j.trsl.2015.09.008
  96. 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. https://doi.org/10.1111/jipb.12152

Cited by

  1. The Conspicuity of CRISPR-Cpf1 System as a Significant Breakthrough in Genome Editing vol.75, pp.1, 2017, https://doi.org/10.1007/s00284-017-1406-8
  2. Duchenne muscular dystrophy: an updated review of common available therapies vol.128, pp.9, 2018, https://doi.org/10.1080/00207454.2018.1430694
  3. The Impact of CRISPR-Cas System on Antiviral Therapy vol.8, pp.4, 2017, https://doi.org/10.15171/apb.2018.067
  4. Recent advancement of engineering microbial hosts for the biotechnological production of flavonoids vol.46, pp.6, 2017, https://doi.org/10.1007/s11033-019-05066-1
  5. Challenges of in vitro genome editing with CRISPR/Cas9 and possible solutions: A review vol.753, pp.None, 2017, https://doi.org/10.1016/j.gene.2020.144813
  6. Genome editing technologies: CRISPR, LEAPER, RESTORE, ARCUT, SATI, and RESCUE vol.20, pp.None, 2017, https://doi.org/10.17179/excli2020-3070
  7. Common therapeutic advances for Duchenne muscular dystrophy (DMD) vol.131, pp.4, 2017, https://doi.org/10.1080/00207454.2020.1740218
  8. Application of CRISPR-Cas9 Editing for Virus Engineering and the Development of Recombinant Viral Vaccines vol.4, pp.4, 2017, https://doi.org/10.1089/crispr.2021.0017
  9. Editing SOX Genes by CRISPR-Cas: Current Insights and Future Perspectives vol.22, pp.21, 2021, https://doi.org/10.3390/ijms222111321