Applications of the CRISPR–Cas9 system in cancer biology (original) (raw)

• Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57–70 (2000).
  CAS PubMed Google Scholar
• Smithies, O., Gregg, R. G., Boggs, S. S., Koralewski, M. A. & Kucherlapati, R. S. Insertion of DNA sequences into the human chromosomal β-globin locus by homologous recombination. Nature 317, 230–234 (1985).
  CAS PubMed Google Scholar
• Thomas, K. R., Folger, K. R. & Capecchi, M. R. High frequency targeting of genes to specific sites in the mammalian genome. Cell 44, 419–428 (1986).
  CAS PubMed Google Scholar
• Mansour, S. L., Thomas, K. R. & Capecchi, M. R. Disruption of the proto-oncogene _Int_-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336, 348–352 (1988).
  CAS PubMed Google Scholar
• Frese, K. K. & Tuveson, D. A. Maximizing mouse cancer models. Nat. Rev. Cancer 7, 645–658 (2007).
  CAS PubMed Google Scholar
• Rudin, N., Sugarman, E. & Haber, J. E. Genetic and physical analysis of double-strand break repair and recombination in Saccharomyces cerevisiae. Genetics 122, 519–534 (1989).
  CAS PubMed PubMed Central Google Scholar
• Plessis, A., Perrin, A., Haber, J. E. & Dujon, B. Site-specific recombination determined by I-SceI, a mitochondrial group I intron-encoded endonuclease expressed in the yeast nucleus. Genetics 130, 451–460 (1992).
  CAS PubMed PubMed Central Google Scholar
• Rouet, P., Smih, F. & Jasin, M. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc. Natl Acad. Sci. USA 91, 6064–6068 (1994).
  CAS PubMed PubMed Central Google Scholar
• Choulika, A., Perrin, A., Dujon, B. & Nicolas, J. F. Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 1968–1973 (1995).
  CAS PubMed PubMed Central Google Scholar
• Bibikova, M., Golic, M., Golic, K. G. & Carroll, D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169–1175 (2002).
  CAS PubMed PubMed Central Google Scholar
• Bibikova, M., Beumer, K., Trautman, J. K. & Carroll, D. Enhancing gene targeting with designed zinc finger nucleases. Science 300, 764 (2003).
  CAS PubMed Google Scholar
• Urnov, F. D. et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nat. Cell Biol. 435, 646–651 (2005).
  CAS Google Scholar
• Christian, M. et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757–761 (2010).
  CAS PubMed PubMed Central Google Scholar
• Li, T. et al. TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res. 39, 359–372 (2011).
  PubMed Google Scholar
• Miller, J. C. et al. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143–148 (2011).
  CAS PubMed Google Scholar
• Hockemeyer, D. et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 29, 731–734 (2011).
  CAS PubMed PubMed Central Google Scholar
• Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S. & Gregory, P. D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636–646 (2010).
  CAS PubMed Google Scholar
• Joung, J. K. & Sander, J. D. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 14, 49–55 (2013).
  CAS PubMed Google Scholar
• Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819–823 (2013).
  CAS PubMed PubMed Central Google Scholar
• Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823–826 (2013).
  CAS PubMed PubMed Central Google Scholar
• Jinek, M. et al. RNA-programmed genome editing in human cells. eLife 2, e00471 (2013).
  PubMed PubMed Central Google Scholar
• Cho, S. W., Kim, S., Kim, J. M. & Kim, J.-S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230–232 (2013).
  CAS PubMed Google Scholar
• Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816–821 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Hsu, P. D. et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827–832 (2013).
  CAS PubMed PubMed Central Google Scholar
• Esvelt, K. M. et al. Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat. Methods 10, 1116–1121 (2013).
  CAS PubMed PubMed Central Google Scholar
• Hou, Z. et al. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl Acad. Sci. USA 110, 15644–15649 (2013).
  CAS PubMed PubMed Central Google Scholar
• Doudna, J. A. & Charpentier, E. Genome editing. The new frontier of genome engineering with CRISPR–Cas9. Science 346, 1258096 (2014).
  PubMed Google Scholar
• Vogelstein, B. et al. Cancer genome landscapes. Science 339, 1546–1558 (2013).
  CAS PubMed PubMed Central Google Scholar
• Denicola, G. M. et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475, 106–109 (2011).
  CAS PubMed PubMed Central Google Scholar
• Kim, S., Kim, D., Cho, S. W., Kim, J. & Kim, J.-S. Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res. 24, 1012–1019 (2014).
  CAS PubMed PubMed Central Google Scholar
• Lin, S., Staahl, B. T., Alla, R. K. & Doudna, J. A. Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. eLife 3, e04766 (2014).
  PubMed PubMed Central Google Scholar
• Malina, A. et al. Repurposing CRISPR/Cas9 for in situ functional assays. Genes Dev. 27, 2602–2614 (2013).
  CAS PubMed PubMed Central Google Scholar
• Shalem, O. et al. Genome-scale CRISPR–Cas9 knockout screening in human cells. Science 343, 84–87 (2014).
  CAS PubMed Google Scholar
• Hsu, P. D., Lander, E. S. & Zhang, F. Development and applications of CRISPR–Cas9 for genome engineering. Cell 157, 1262–1278 (2014).
  CAS PubMed PubMed Central Google Scholar
• Heyer, J., Kwong, L. N., Lowe, S. W. & Chin, L. Non-germline genetically engineered mouse models for translational cancer research. Nat. Rev. Cancer 10, 470–480 (2010).
  CAS PubMed PubMed Central Google Scholar
• Engelman, J. A. et al. Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat. Med. 14, 1351–1356 (2008).
  CAS PubMed PubMed Central Google Scholar
• Chen, Z. et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature 483, 613–617 (2012).
  CAS PubMed PubMed Central Google Scholar
• Wang, H. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910–918 (2013).
  CAS PubMed PubMed Central Google Scholar
• Yang, H. et al. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370–1379 (2013).
  CAS PubMed PubMed Central Google Scholar
• Jackson, E. L. et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15, 3243–3248 (2001).
  CAS PubMed PubMed Central Google Scholar
• Guerra, C. et al. Tumor induction by an endogenous K-ras oncogene is highly dependent on cellular context. Cancer Cell 4, 111–120 (2003).
  CAS PubMed Google Scholar
• Findlay, G. M., Boyle, E. A., Hause, R. J., Klein, J. C. & Shendure, J. Saturation editing of genomic regions by multiplex homology-directed repair. Nature 513, 120–123 (2014).
  CAS PubMed PubMed Central Google Scholar
• Dow, L. E. & Lowe, S. W. Life in the fast lane: mammalian disease models in the genomics era. Cell 148, 1099–1109 (2012).
  CAS PubMed PubMed Central Google Scholar
• Chen, C. et al. MLL3 is a haploinsufficient 7q tumor suppressor in acute myeloid leukemia. Cancer Cell 25, 652–665 (2014).
  PubMed PubMed Central Google Scholar
• Heckl, D. et al. Generation of mouse models of myeloid malignancy with combinatorial genetic lesions using CRISPR–Cas9 genome editing. Nat. Biotechnol. 32, 941–946 (2014).
  CAS PubMed PubMed Central Google Scholar
• Xue, W. et al. CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514, 380–384 (2014).
  CAS PubMed PubMed Central Google Scholar
• Jackson, E. et al. The differential effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res. 65, 10280–10288 (2005).
  CAS PubMed Google Scholar
• Sanchez-Rivera, F. J. et al. Rapid modelling of cooperating genetic events in cancer through somatic genome editing. Nature 516, 428–431 (2014).
  CAS PubMed PubMed Central Google Scholar
• Maddalo, D. et al. In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 516, 423–427 (2014).
  CAS PubMed PubMed Central Google Scholar
• Soda, M. et al. Identification of the transforming EML4_–_ALK fusion gene in non-small-cell lung cancer. Nature 448, 561–566 (2007).
  CAS PubMed Google Scholar
• Shaw, A. T. et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N. Engl. J. Med. 368, 2385–2394 (2013).
  CAS PubMed Google Scholar
• Blasco, R. B. et al. Simple and rapid in vivo generation of chromosomal rearrangements using CRISPR/Cas9 technology. Cell Rep. 9, 1219–1227 (2014).
  CAS PubMed Google Scholar
• Zuris, J. A. et al. Cationic lipid-mediated delivery of proteins enables efficient protein-based genome editing in vitro and in vivo. Nat. Biotechnol. 33, 73–80 (2015).
  CAS PubMed Google Scholar
• Platt, R. J. et al. CRISPR–Cas9 knockin mice for genome editing and cancer modeling. Cell 159, 440–455 (2014).
  CAS PubMed PubMed Central Google Scholar
• Yin, H. et al. Non-viral vectors for gene-based therapy. Nat. Rev. Genet. 15, 541–555 (2014).
  CAS PubMed Google Scholar
• Dow, L. E. et al. Inducible in vivo genome editing with CRISPR–Cas9. Nat. Biotechnol. 33, 390–394 (2015).
  CAS PubMed PubMed Central Google Scholar
• Tanenbaum, M. E., Gilbert, L. A., Qi, L. S., Weissman, J. S. & Vale, R. D. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159, 635–646 (2014).
  CAS PubMed PubMed Central Google Scholar
• Gilbert, L. A. et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154, 442–451 (2013).
  CAS PubMed PubMed Central Google Scholar
• Whitworth, K. M. et al. Use of the CRISPR/Cas9 system to produce genetically engineered pigs from _in vitro_-derived oocytes and embryos. Biol. Reprod. 91, 78 (2014).
  PubMed PubMed Central Google Scholar
• Niu, Y. et al. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156, 836–843 (2014).
  CAS PubMed Google Scholar
• Crystal, A. S. et al. Patient-derived models of acquired resistance can identify effective drug combinations for cancer. Science 346, 1480–1486 (2014).
  CAS PubMed PubMed Central Google Scholar
• Yin, H. et al. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat. Biotechnol. 32, 551–553 (2014).
  CAS PubMed PubMed Central Google Scholar
• Sadelain, M., Brentjens, R. & Rivière, I. The basic principles of chimeric antigen receptor design. Cancer Discov. 3, 388–398 (2013).
  CAS PubMed PubMed Central Google Scholar
• Sadelain, M., Papapetrou, E. P. & Bushman, F. D. Safe harbours for the integration of new DNA in the human genome. Nat. Rev. Cancer 12, 51–58 (2012).
  CAS Google Scholar
• Bikard, D. et al. Programmable repression and activation of bacterial gene expression using an engineered CRISPR–Cas system. Nucleic Acids Res. 41, 7429–7437 (2013).
  CAS PubMed PubMed Central Google Scholar
• Gilbert, L. A. et al. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159, 647–661 (2014).
  CAS PubMed PubMed Central Google Scholar
• Mali, P. et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833–838 (2013).
  CAS PubMed PubMed Central Google Scholar
• Perez-Pinera, P. et al. RNA-guided gene activation by CRISPR–Cas9-based transcription factors. Nat. Methods 10, 973–976 (2013).
  CAS PubMed PubMed Central Google Scholar
• Cheng, A. W. et al. Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res. 23, 1163–1171 (2013).
  CAS PubMed PubMed Central Google Scholar
• Maeder, M. L. et al. CRISPR RNA-guided activation of endogenous human genes. Nat. Methods 10, 977–979 (2013).
  CAS PubMed PubMed Central Google Scholar
• Konermann, S. et al. Genome-scale transcriptional activation by an engineered CRISPR–Cas9 complex. Nature 517, 583–588 (2014).
  PubMed PubMed Central Google Scholar
• Zalatan, J. G. et al. Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell 160, 339–350 (2015).
  CAS PubMed Google Scholar
• Wang, T., Wei, J. J., Sabatini, D. M. & Lander, E. S. Genetic screens in human cells using the CRISPR–Cas9 system. Science 343, 80–84 (2014).
  CAS PubMed Google Scholar
• Koike-Yusa, H., Li, Y., Tan, E.-P., Velasco-Herrera, M. D. C. & Yusa, K. Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat. Biotechnol. 32, 267–273 (2013).
  PubMed Google Scholar
• Zhou, Y. et al. High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature 509, 487–491 (2014).
  CAS PubMed Google Scholar
• Chen, S. et al. Genome-wide CRISPR screen in a mouse model of tumor growth and metastasis. Cell 160, 1246–1260 (2015).
  CAS PubMed PubMed Central Google Scholar
• Matano, M. et al. Modeling colorectal cancer using CRISPR–Cas9-mediated engineering of human intestinal organoids. Nat. Med. 21, 256–262 (2015).
  CAS PubMed Google Scholar
• Mansour, M. R. et al. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science 346, 1373–1377 (2014).
  CAS PubMed PubMed Central Google Scholar
• Choi, P. S. & Meyerson, M. Targeted genomic rearrangements using CRISPR/Cas technology. Nat. Commun. 5, 3728 (2014).
  CAS PubMed Google Scholar
• Torres, R. et al. Engineering human tumour-associated chromosomal translocations with the RNA-guided CRISPR–Cas9 system. Nat. Commun. 5, 3964 (2014).
  CAS PubMed Google Scholar
• Ghezraoui, H. et al. Chromosomal translocations in human cells are generated by canonical nonhomologous end-joining. Mol. Cell 55, 829–842 (2014).
  CAS PubMed PubMed Central Google Scholar
• Xiao, A. et al. Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res. 41, e141 (2013).
  CAS PubMed PubMed Central Google Scholar
• Canver, M. C. et al. Characterization of genomic deletion efficiency mediated by clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 nuclease system in mammalian cells. J. Biol. Chem. 289, 21312–21324 (2014).
  PubMed PubMed Central Google Scholar
• Han, J. et al. Efficient in vivo deletion of a large imprinted lncRNA by CRISPR/Cas9. RNA Biol. 11, 829–835 (2014).
  CAS PubMed PubMed Central Google Scholar
• Ho, T.-T. et al. Targeting non-coding RNAs with the CRISPR/Cas9 system in human cell lines. Nucleic Acids Res. 43, e17 (2014).
  PubMed PubMed Central Google Scholar
• Essletzbichler, P. et al. Megabase-scale deletion using CRISPR/Cas9 to generate a fully haploid human cell line. Genome Res. 24, 2059–2065 (2014).
  CAS PubMed PubMed Central Google Scholar