1932

Abstract

In just a few short years, CRISPR/Cas9 genome editing has fundamentally changed basic, agricultural, and biomedical research, but no field has felt a more profound impact than cancer research. The ability to quickly and precisely manipulate the genome has opened the floodgates for a new and more elaborate understanding of how genes and gene regulation influence disease. Here we review how the development and implementation of CRISPR-based technology is redefining the way we study cancer, and ultimately how it may be used to improve treatment outcomes.

Keyword(s): cancerCas9CRISPRgenome editingin vivo
Loading

Article metrics loading...

/content/journals/10.1146/annurev-cancerbio-030617-050455
2018-03-04
2024-10-13
Loading full text...

Full text loading...

/deliver/fulltext/cancerbio/2/1/annurev-cancerbio-030617-050455.html?itemId=/content/journals/10.1146/annurev-cancerbio-030617-050455&mimeType=html&fmt=ahah

Literature Cited

  1. Abbosh C, Birkbak NJ, Wilson GA, Jamal-Hanjani M, Constantin T. et al. 2017. Phylogenetic ctDNA analysis depicts early stage lung cancer evolution. Nature 545:446–51 [Google Scholar]
  2. Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM. et al. 2016. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573 [Google Scholar]
  3. Adamson B, Norman TM, Jost M, Cho MY, Nunez JK. et al. 2016. A multiplexed single-cell CRISPR screening platform enables systematic dissection of the unfolded protein response. Cell 167:1867–82.e21 [Google Scholar]
  4. Andersson-Rolf A, Mustata RC, Merenda A, Kim J, Perera S. et al. 2017. One-step generation of conditional and reversible gene knockouts. Nat. Methods 14:287–89 [Google Scholar]
  5. Annunziato S, Kas SM, Nethe M, Yucel H, Del Bravo J. et al. 2016. Modeling invasive lobular breast carcinoma by CRISPR/Cas9-mediated somatic genome editing of the mammary gland. Genes Dev 30:1470–80 [Google Scholar]
  6. Bengtsson NE, Hall JK, Odom GL, Phelps MP, Andrus CR. et al. 2017. Muscle-specific CRISPR/Cas9 dystrophin gene editing ameliorates pathophysiology in a mouse model for Duchenne muscular dystrophy. Nat. Commun. 8:14454 [Google Scholar]
  7. Blasco RB, Karaca E, Ambrogio C, Cheong T-C, Karayol E. et al. 2014. Simple and rapid in vivo generation of chromosomal rearrangements using CRISPR/Cas9 technology. Cell Rep 9:1219–27 [Google Scholar]
  8. Bouabe H, Okkenhaug K. 2013. Gene targeting in mice: a review. Methods Mol. Biol. 1064:315–36 [Google Scholar]
  9. Canver MC, Smith EC, Sher F, Pinello L, Sanjana NE. et al. 2015. BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis. Nature 527:192–97 [Google Scholar]
  10. Capecchi MR. 2005. Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century. Nat. Rev. Genet. 6:507–12 [Google Scholar]
  11. Chang H, Yi B, Ma R, Zhang X, Zhao H, Xi Y. 2016. CRISPR/cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Sci. Rep. 6:22312 [Google Scholar]
  12. Chen S, Sanjana NE, Zheng K, Shalem O, Lee K. et al. 2015. Genome-wide CRISPR screen in a mouse model of tumor growth and metastasis. Cell 160:1246–60 [Google Scholar]
  13. Chiou SH, Winters IP, Wang J, Naranjo S, Dudgeon C. et al. 2015. Pancreatic cancer modeling using retrograde viral vector delivery and in vivo CRISPR/Cas9-mediated somatic genome editing. Genes Dev 29:1576–85 [Google Scholar]
  14. Choi PS, Meyerson M. 2014. Targeted genomic rearrangements using CRISPR/Cas technology. Nat. Commun. 5:3728 [Google Scholar]
  15. Chu VT, Weber T, Wefers B, Wurst W, Sander S. et al. 2015. Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat. Biotechnol. 33:543–48 [Google Scholar]
  16. Cong L, Ran FA, Cox D, Lin S, Barretto R. et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–23 [Google Scholar]
  17. Cook PJ, Thomas R, Kannan R, de Leon ES, Drilon A. et al. 2017. Somatic chromosomal engineering identifies BCAN-NTRK1 as a potent glioma driver and therapeutic target. Nat. Commun. 8:15987 [Google Scholar]
  18. Datlinger P, Rendeiro AF, Schmidl C, Krausgruber T, Traxler P. et al. 2017. Pooled CRISPR screening with single-cell transcriptome readout. Nat. Methods 14:297–301 [Google Scholar]
  19. de Wit E, Vos ES, Holwerda SJ, Valdes-Quezada C, Verstegen MJ. et al. 2015. CTCF binding polarity determines chromatin looping. Mol. Cell 60:676–84 [Google Scholar]
  20. Dever DP, Bak RO, Reinisch A, Camarena J, Washington G. et al. 2016. CRISPR/Cas9 β-globin gene targeting in human haematopoietic stem cells. Nature 539:384–89 [Google Scholar]
  21. Dixit A, Parnas O, Li B, Chen J, Fulco CP. et al. 2016. Perturb-seq: dissecting molecular circuits with scalable single-cell RNA profiling of pooled genetic screens. Cell 167:1853–66.e17 [Google Scholar]
  22. Dominguez AA, Lim WA, Qi LS. 2016. Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation. Nat. Rev. Mol. Cell Biol. 17:5–15 [Google Scholar]
  23. Dow LE. 2015. Modeling disease in vivo with CRISPR/Cas9. Trends Mol. Med. 21:609–21 [Google Scholar]
  24. Dow LE, Fisher J, O'Rourke KP, Muley A, Kastenhuber ER. et al. 2015. Inducible in vivo genome editing with CRISPR-Cas9. Nat. Biotechnol. 33:390–94 [Google Scholar]
  25. Drost J, van Jaarsveld RH, Ponsioen B, Zimberlin C, van Boxtel R. et al. 2015. Sequential cancer mutations in cultured human intestinal stem cells. Nature 521:43–47 [Google Scholar]
  26. East-Seletsky A, O'Connell MR, Knight SC, Burstein D, Cate JH. et al. 2016. Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature 538:270–73 [Google Scholar]
  27. Eyquem J, Mansilla-Soto J, Giavridis T, van der Stegen SJ, Hamieh M. et al. 2017. Targeting a CAR to the TRAC locus with CRISPR/Cas9 enhances tumour rejection. Nature 543:113–17 [Google Scholar]
  28. Fearon ER, Vogelstein B. 1990. A genetic model for colorectal tumorigenesis. Cell 61:759–67 [Google Scholar]
  29. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D. et al. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31:822–26 [Google Scholar]
  30. Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32:279–84 [Google Scholar]
  31. Gantz VM, Jasinskiene N, Tatarenkova O, Fazekas A, Macias VM. et al. 2015. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. PNAS 112:E6736–43 [Google Scholar]
  32. Ghezraoui H, Piganeau M, Renouf B, Renaud JB, Sallmyr A. et al. 2014. Chromosomal translocations in human cells are generated by canonical nonhomologous end-joining. Mol. Cell 55:829–42 [Google Scholar]
  33. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y. et al. 2014. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159:647–61 [Google Scholar]
  34. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA. et al. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–51 [Google Scholar]
  35. Gootenberg JS, Abudayyeh OO, Lee JW, Essletzbichler P, Dy AJ. et al. 2017. Nucleic acid detection with CRISPR-Cas13a/C2c2. Science 356:438–42 [Google Scholar]
  36. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinform 8:172 [Google Scholar]
  37. Guo X, Zhang T, Hu Z, Zhang Y, Shi Z. et al. 2014. Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development 141:707–14 [Google Scholar]
  38. Guo Y, Xu Q, Canzio D, Shou J, Li J. et al. 2015. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162:900–10 [Google Scholar]
  39. Gutschner T, Haemmerle M, Genovese G, Draetta GF, Chin L. 2016. Post-translational regulation of Cas9 during G1 enhances homology-directed repair. Cell Rep 14:1555–66 [Google Scholar]
  40. Hammond A, Galizi R, Kyrou K, Simoni A, Siniscalchi C. et al. 2016. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat. Biotechnol. 34:78–83 [Google Scholar]
  41. Han T, Schatoff EM, Murphy C, Zafra MP, Wilkinson JE. et al. 2017. R-Spondin chromosome rearrangements drive Wnt-dependent tumour initiation and maintenance in the intestine. Nat. Commun. 8:15945 [Google Scholar]
  42. Heckl D, Kowalczyk MS, Yudovich D, Belizaire R, Puram RV. et al. 2014. Generation of mouse models of myeloid malignancy with combinatorial genetic lesions using CRISPR-Cas9 genome editing. Nat. Biotechnol. 32:941–46 [Google Scholar]
  43. Hess GT, Fresard L, Han K, Lee CH, Li A. et al. 2016. Directed evolution using dCas9-targeted somatic hypermutation in mammalian cells. Nat. Methods 13:1036–42 [Google Scholar]
  44. Hilton IB, D'Ippolito AM, Vockley CM, Thakore PI, Crawford GE. et al. 2015. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33:510–17 [Google Scholar]
  45. Howden SE, Maufort JP, Duffin BM, Elefanty AG, Stanley EG, Thomson JA. 2015. Simultaneous reprogramming and gene correction of patient fibroblasts. Stem Cell Rep 5:1109–18 [Google Scholar]
  46. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A. 1987. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169:5429–33 [Google Scholar]
  47. Jaitin DA, Weiner A, Yofe I, Lara-Astiaso D, Keren-Shaul H. et al. 2016. Dissecting immune circuits by linking CRISPR-pooled screens with single-cell RNA-seq. Cell 167:1883–96.e15 [Google Scholar]
  48. Jamal-Hanjani M, Wilson GA, McGranahan N, Birkbak NJ, Watkins TBK. et al. 2017. Tracking the evolution of non-small-cell lung cancer. N. Engl. J. Med. 376:2109–21 [Google Scholar]
  49. Jao L-E, Wente SR, Chen W. 2013. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. PNAS 110:13904–9 [Google Scholar]
  50. 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 337:816–21 [Google Scholar]
  51. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. 2013. RNA-programmed genome editing in human cells. eLife 2:e00471 [Google Scholar]
  52. Katigbak A, Cencic R, Robert F, Senecha P, Scuoppo C, Pelletier J. 2016. A CRISPR/Cas9 functional screen identifies rare tumor suppressors. Sci. Rep. 6:38968 [Google Scholar]
  53. Kearns NA, Pham H, Tabak B, Genga RM, Silverstein NJ. et al. 2015. Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat. Methods 12:401–3 [Google Scholar]
  54. Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT. et al. 2016.a High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529:490–95 [Google Scholar]
  55. Kleinstiver BP, Prew MS, Tsai SQ, Nguyen NT, Topkar VV. et al. 2015.a Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat. Biotechnol. 33:1293–98 [Google Scholar]
  56. Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT. et al. 2015.b Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523:481–85 [Google Scholar]
  57. Kleinstiver BP, Tsai SQ, Prew MS, Nguyen NT, Welch MM. et al. 2016.b Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat. Biotechnol. 34:869–74 [Google Scholar]
  58. Kochenderfer JN, Rosenberg SA. 2013. Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors. Nat. Rev. Clin. Oncol. 10:267–76 [Google Scholar]
  59. 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 533:420–24 [Google Scholar]
  60. Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO. et al. 2015. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517:583–88 [Google Scholar]
  61. Korkmaz G, Lopes R, Ugalde AP, Nevedomskaya E, Han R. et al. 2016. Functional genetic screens for enhancer elements in the human genome using CRISPR-Cas9. Nat. Biotechnol. 34:192–98 [Google Scholar]
  62. Kraft K, Geuer S, Will AJ, Chan WL, Paliou C. et al. 2015. Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice. Cell Rep 34:192–98 [Google Scholar]
  63. Kurata M, Rathe SK, Bailey NJ, Aumann NK, Jones JM. et al. 2016. Using genome-wide CRISPR library screening with library resistant DCK to find new sources of Ara-C drug resistance in AML. Sci. Rep. 6:36199 [Google Scholar]
  64. Lekomtsev S, Aligianni S, Lapao A, Burckstummer T. 2016. Efficient generation and reversion of chromosomal translocations using CRISPR/Cas technology. BMC Genom 17:739 [Google Scholar]
  65. Li HL, Fujimoto N, Sasakawa N, Shirai S, Ohkame T. et al. 2015. Precise correction of the dystrophin gene in duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9. Stem Cell Rep 4:143–54 [Google Scholar]
  66. Li Y, Park AI, Mou H, Colpan C, Bizhanova A. et al. 2015. A versatile reporter system for CRISPR-mediated chromosomal rearrangements. Genome Biol 16:111 [Google Scholar]
  67. 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 [Google Scholar]
  68. Liu SJ, Horlbeck MA, Cho SW, Birk HS, Malatesta M. et al. 2017. CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells. Science 355:aah7111 [Google Scholar]
  69. Liu XS, Wu H, Ji X, Stelzer Y, Wu X. et al. 2016. Editing DNA methylation in the mammalian genome. Cell 167:233–47.e17 [Google Scholar]
  70. Long C, Amoasii L, Mireault AA, McAnally JR, Li H. et al. 2016. Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351:400–3 [Google Scholar]
  71. Lupianez DG, Kraft K, Heinrich V, Krawitz P, Brancati F. et al. 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–25 [Google Scholar]
  72. Ma Y, Shen B, Zhang X, Lu Y, Chen W. et al. 2014. Heritable multiplex genetic engineering in rats using CRISPR/Cas9. PLOS ONE 9:e89413 [Google Scholar]
  73. Ma Y, Zhang J, Yin W, Zhang Z, Song Y, Chang X. 2016. Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat. Methods 13:1029–35 [Google Scholar]
  74. Maddalo D, Manchado E, Concepcion CP, Bonetti C, Vidigal JA. et al. 2014. In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 516:423–27 [Google Scholar]
  75. Maddalo D, Ventura A. 2016. Somatic engineering of oncogenic chromosomal rearrangements: a perspective. Cancer Res 76:4918–23 [Google Scholar]
  76. Mali P, Yang L, Esvelt KM, Aach J, Guell M. et al. 2013. RNA-guided human genome engineering via Cas9. Science 339:823–26 [Google Scholar]
  77. Maresch R, Mueller S, Veltkamp C, Ollinger R, Friedrich M. et al. 2016. Multiplexed pancreatic genome engineering and cancer induction by transfection-based CRISPR/Cas9 delivery in mice. Nat. Commun. 7:10770 [Google Scholar]
  78. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11:181–90 [Google Scholar]
  79. 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. 33:538–42 [Google Scholar]
  80. Matano M, Date S, Shimokawa M, Takano A, Fujii M. et al. 2015. Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat. Med. 21:256–62 [Google Scholar]
  81. Munoz DM, Cassiani PJ, Li L, Billy E, Korn JM. et al. 2016. CRISPR screens provide a comprehensive assessment of cancer vulnerabilities but generate false-positive hits for highly amplified genomic regions. Cancer Discov 6:900–13 [Google Scholar]
  82. Nelson CE, Hakim CH, Ousterout DG, Thakore PI, Moreb EA. et al. 2016. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:403–7 [Google Scholar]
  83. Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M. et al. 2016. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353:aaf8729 [Google Scholar]
  84. Niu Y, Shen B, Cui Y, Chen Y, Wang J. et al. 2014. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156:836–43 [Google Scholar]
  85. Oliver D, Yuan S, McSwiggin H, Yan W. 2015. Pervasive genotypic mosaicism in founder mice derived from genome editing through pronuclear injection. PLOS ONE 10:e0129457 [Google Scholar]
  86. O'Rourke KP, Loizou E, Livshits G, Schatoff EM, Baslan T. et al. 2017. Transplantation of engineered organoids enables rapid generation of metastatic mouse models of colorectal cancer. Nat. Biotechnol. 35:577–82 [Google Scholar]
  87. Paquet D, Kwart D, Chen A, Sproul A, Jacob S. et al. 2016. Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9. Nature 533:125–29 [Google Scholar]
  88. Pardee K, Green AA, Takahashi MK, Braff D, Lambert G. et al. 2016. Rapid, low-cost detection of Zika virus using programmable biomolecular components. Cell 165:1255–66 [Google Scholar]
  89. Park CY, Kim DH, Son JS, Sung JJ, Lee J. et al. 2015. Functional correction of large factor VIII gene chromosomal inversions in hemophilia A patient-derived iPSCs using CRISPR-Cas9. Cell Stem Cell 17:213–20 [Google Scholar]
  90. Parnas O, Jovanovic M, Eisenhaure TM, Herbst RH, Dixit A. et al. 2015. A genome-wide CRISPR screen in primary immune cells to dissect regulatory networks. Cell 162:675–86 [Google Scholar]
  91. Perez AR, Pritykin Y, Vidigal JA, Chhangawala S, Zamparo L. et al. 2017. GuideScan software for improved single and paired CRISPR guide RNA design. Nat. Biotechnol. 35:347–49 [Google Scholar]
  92. Platt RJ, Chen S, Zhou Y, Yim MJ, Swiech L. et al. 2014. CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159:440–55 [Google Scholar]
  93. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS. et al. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–83 [Google Scholar]
  94. Radzisheuskaya A, Shlyueva D, Muller I, Helin K. 2016. Optimizing sgRNA position markedly improves the efficiency of CRISPR/dCas9-mediated transcriptional repression. Nucleic Acids Res 44:e141 [Google Scholar]
  95. Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS. et al. 2015. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520:186–91 [Google Scholar]
  96. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8:2281–308 [Google Scholar]
  97. 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. 34:339–44 [Google Scholar]
  98. Roper J, Tammela T, Cetinbas NM, Akkad A, Roghanian A. et al. 2017. In vivo genome editing and organoid transplantation models of colorectal cancer and metastasis. Nat. Biotechnol. 35:569–76 [Google Scholar]
  99. Sanchez-Rivera FJ, Papagiannakopoulos T, Romero R, Tammela T, Bauer MR. et al. 2014. Rapid modelling of cooperating genetic events in cancer through somatic genome editing. Nature 516:428–31 [Google Scholar]
  100. Sanjana NE, Wright J, Zheng K, Shalem O, Fontanillas P. et al. 2016. High-resolution interrogation of functional elements in the noncoding genome. Science 353:1545–49 [Google Scholar]
  101. Schwank G, Koo BK, Sasselli V, Dekkers JF, Heo I. et al. 2013. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 13:653–58 [Google Scholar]
  102. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA. et al. 2014. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87 [Google Scholar]
  103. Shan Q, Wang Y, Li J, Zhang Y, Chen K. et al. 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31:686–88 [Google Scholar]
  104. Shi J, Wang E, Milazzo JP, Wang Z, Kinney JB, Vakoc CR. 2015. Discovery of cancer drug targets by CRISPR-Cas9 screening of protein domains. Nat. Biotechnol. 33:661–67 [Google Scholar]
  105. Shimokawa M, Ohta Y, Nishikori S, Matano M, Takano A. et al. 2017. Visualization and targeting of LGR5+ human colon cancer stem cells. Nature 545:187–92 [Google Scholar]
  106. Singh D, Sternberg SH, Fei J, Doudna JA, Ha T. 2016. Real-time observation of DNA recognition and rejection by the RNA-guided endonuclease Cas9. Nat. Commun. 7:12778 [Google Scholar]
  107. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. 2016. Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88 [Google Scholar]
  108. Soldner F, Stelzer Y, Shivalila CS, Abraham BJ, Latourelle JC. et al. 2016. Parkinson-associated risk variant in distal enhancer of α-synuclein modulates target gene expression. Nature 533:95–99 [Google Scholar]
  109. Spraggon L, Martelotto LG, Hmeljak J, Hitchman TD, Wang J. et al. 2017. Generation of conditional oncogenic chromosomal translocations using CRISPR-Cas9 genomic editing and homology-directed repair. J. Pathol. 242:102–12 [Google Scholar]
  110. Staahl BT, Benekareddy M, Coulon-Bainier C, Banfal AA, Floor SN. et al. 2017. Efficient genome editing in the mouse brain by local delivery of engineered Cas9 ribonucleoprotein complexes. Nat. Biotechnol. 35:431–34 [Google Scholar]
  111. Steinhart Z, Pavlovic Z, Chandrashekhar M, Hart T, Wang X. et al. 2017. Genome-wide CRISPR screens reveal a Wnt-FZD5 signaling circuit as a druggable vulnerability of RNF43-mutant pancreatic tumors. Nat. Med. 23:60–68 [Google Scholar]
  112. Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA. 2014. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62–67 [Google Scholar]
  113. Sur S, Pagliarini R, Bunz F, Rago C, Diaz LA Jr.. et al. 2009. A panel of isogenic human cancer cells suggests a therapeutic approach for cancers with inactivated p53. PNAS 106:3964–69 [Google Scholar]
  114. Tabebordbar M, Zhu K, Cheng JK, Chew WL, Widrick JJ. et al. 2016. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351:407–11 [Google Scholar]
  115. Tsai SQ, Zheng Z, Nguyen NT, Liebers M, Topkar VV. et al. 2015. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat. Biotechnol. 33:187–97 [Google Scholar]
  116. Van Dyke T, Jacks T. 2002. Cancer modeling in the modern era: progress and challenges. Cell 108:135–44 [Google Scholar]
  117. van Overbeek M, Capurso D, Carter MM, Thompson MS, Frias E. et al. 2016. DNA repair profiling reveals nonrandom outcomes at Cas9-mediated breaks. Mol. Cell 63:633–46 [Google Scholar]
  118. Vanoli F, Tomishima M, Feng W, Lamribet K, Babin L. et al. 2017. CRISPR-Cas9-guided oncogenic chromosomal translocations with conditional fusion protein expression in human mesenchymal cells. PNAS 114:3696–701 [Google Scholar]
  119. Vidigal JA, Ventura A. 2015. Rapid and efficient one-step generation of paired gRNA CRISPR/Cas9 libraries. Nat. Commun. 6:8083 [Google Scholar]
  120. Vojta A, Dobrinic P, Tadic V, Bockor L, Korac P. et al. 2016. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res 44:5615–28 [Google Scholar]
  121. Wan H, Feng C, Teng F, Yang S, Hu B. et al. 2015. One-step generation of p53 gene biallelic mutant Cynomolgus monkey via the CRISPR/Cas system. Cell Res 25:258–61 [Google Scholar]
  122. Wang D, Mou H, Li S, Li Y, Hough S. et al. 2015. Adenovirus-mediated somatic genome editing of Pten by CRISPR/Cas9 in mouse liver in spite of Cas9-specific immune responses. Hum. Gene. Ther. 26:432–42 [Google Scholar]
  123. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW. et al. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–18 [Google Scholar]
  124. Wang T, Wei JJ, Sabatini DM, Lander ES. 2014. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343:80–84 [Google Scholar]
  125. Weber J, Ollinger R, Friedrich M, Ehmer U, Barenboim M. et al. 2015. CRISPR/Cas9 somatic multiplex-mutagenesis for high-throughput functional cancer genomics in mice. PNAS 112:13982–87 [Google Scholar]
  126. Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW. et al. 2015. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33:1162–64 [Google Scholar]
  127. Xue W, Chen S, Yin H, Tammela T, Papagiannakopoulos T. et al. 2014. CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514:380–84 [Google Scholar]
  128. Yang D, Scavuzzo MA, Chmielowiec J, Sharp R, Bajic A, Borowiak M. 2016. Enrichment of G2/M cell cycle phase in human pluripotent stem cells enhances HDR-mediated gene repair with customizable endonucleases. Sci. Rep. 6:21264 [Google Scholar]
  129. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. 2013. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154:1370–79 [Google Scholar]
  130. Yen ST, Zhang M, Deng JM, Usman SJ, Smith CN. et al. 2014. Somatic mosaicism and allele complexity induced by CRISPR/Cas9 RNA injections in mouse zygotes. Dev. Biol. 393:3–9 [Google Scholar]
  131. Yin H, Xue W, Chen S, Bogorad RL, Benedetti E. et al. 2014. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat. Biotechnol. 32:551–53 [Google Scholar]
  132. Yin L, Maddison LA, Li M, Kara N, LaFave MC. et al. 2015. Multiplex conditional mutagenesis using transgenic expression of Cas9 and sgRNAs. Genetics 200:431–41 [Google Scholar]
  133. Yu C, Liu Y, Ma T, Liu K, Xu S. et al. 2015. Small molecules enhance CRISPR genome editing in pluripotent stem cells. Cell Stem Cell 16:142–47 [Google Scholar]
  134. Yun J, Rago C, Cheong I, Pagliarini R, Angenendt P. et al. 2009. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science 325:1555–59 [Google Scholar]
  135. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS. et al. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–71 [Google Scholar]
  136. Zhao Y, Dai Z, Liang Y, Yin M, Ma K. et al. 2014. Sequence-specific inhibition of microRNA via CRISPR/CRISPRi system. Sci. Rep. 4:3943 [Google Scholar]
  137. Zhou J, Shen B, Zhang W, Wang J, Yang J. et al. 2014. One-step generation of different immunodeficient mice with multiple gene modifications by CRISPR/Cas9 mediated genome engineering. Int. J. Biochem. Cell Biol. 46:49–55 [Google Scholar]
  138. Zhu S, Li W, Liu J, Chen CH, Liao Q. et al. 2016. Genome-scale deletion screening of human long non-coding RNAs using a paired-guide RNA CRISPR–Cas9 library. Nat. Biotechnol. 34:1279–86 [Google Scholar]
  139. Zuckermann M, Hovestadt V, Knobbe-Thomsen CB, Zapatka M, Northcott PA. et al. 2015. Somatic CRISPR/Cas9-mediated tumour suppressor disruption enables versatile brain tumour modelling. Nat. Commun. 6:7391 [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-030617-050455
Loading
/content/journals/10.1146/annurev-cancerbio-030617-050455
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error