Rapid generation of drug-resistance alleles at endogenous loci using CRISPR-Cas9 indel mutagenesis

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Ipsaro, Jonathan J ^a   Shen, Chen ^a   Arai, Eri ^b   Xu, Yali ^a,c   Kinney, Justin B ^a   Joshua Tor, Leemor ^a,d   Vakoc, Christopher R ^a   Shi, Junwei ^b  

^a Simons Center for Quantitative Biology   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISRUPTOR OF TELOMERIC SILENCING 1 LIKE PROTEIN; ENZYME; HISTONE METHYLTRANSFERASE; MIXED LINEAGE LEUKEMIA PROTEIN; TAZEMETOSTAT; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR HOXA9; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BENZIMIDAZOLE DERIVATIVE; DOT1L PROTEIN, HUMAN; EPZ-5676; EZH2 PROTEIN, HUMAN; METHYLTRANSFERASE;

ALLELE; ANIMAL CELL; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; CRISPR CAS SYSTEM; DISRUPTOR OF TELOMERIC SILENCING 1 LIKE GENE; DNA CLEAVAGE; ENZYME ACTIVITY; GENE LOCUS; GENETIC CODE; GENETIC SCREENING; HISTONE METHYLTRANSFERASE GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; INDEL MUTATION; LEUKEMIA CELL; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; TRANSCRIPTION FACTOR EZH2 GENE; WILD TYPE; ANIMAL; CELL LINE; CELL PROLIFERATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR MODEL; MOUSE; NEOPLASMS; TUMOR CELL LINE;

ALLELES; ANIMALS; ANTINEOPLASTIC AGENTS; BENZIMIDAZOLES; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; DRUG RESISTANCE, NEOPLASM; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; HEK293 CELLS; HUMANS; INDEL MUTATION; METHYLTRANSFERASES; MICE; MODELS, MOLECULAR; MUTAGENESIS; NEOPLASMS;

EID: 85013798316     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0172177     Document Type: Article

References (32)

1. Azam M, Latek RR, Daley GQ (2003) Mechanisms of autoinhibition and STI-571/imatinib resistance revealed by mutagenesis of BCR-ABL. Cell 112: 831-843. PMID: 12654249
2. Botstein D, Shortle D (1985) Strategies and applications of in vitro mutagenesis. Science 229: 1193-1201. PMID: 2994214
3. Poulikakos PI, Persaud Y, Janakiraman M, Kong X, Ng C, et al. (2011) RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 480: 387-390. doi: 10.1038/ nature10662 PMID: 22113612
4. Foster SA, Whalen DM, Ozen A, Wongchenko MJ, Yin J, et al. (2016) Activation Mechanism of Oncogenic Deletion Mutations in BRAF, EGFR, and HER2. Cancer Cell 29: 477-493. doi: 10.1016/j.ccell. 2016.02.010 PMID: 26996308
5. Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157: 1262-1278. doi: 10.1016/j.cell.2014.05.010 PMID: 24906146
6. Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346: 1258096. doi: 10.1126/science.1258096 PMID: 25430774
7. Cong L, Ran FA, Cox D, Lin S, Barretto R, et al. (2013) Multiplex genome engineering using CRISPR/ Cas systems. Science 339: 819-823. doi: 10.1126/science.1231143 PMID: 23287718
8. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, et al. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821. doi: 10.1126/science.1225829 PMID: 22745249
9. Mali P, Yang L, Esvelt KM, Aach J, Guell M, et al. (2013) RNA-guided human genome engineering via Cas9. Science 339: 823-826. doi: 10.1126/science.1232033 PMID: 23287722
10. Jasin M, Haber JE (2016) The democratization of gene editing: Insights from site-specific cleavage and double-strand break repair. DNA Repair (Amst).
11. Shi J, Wang E, Milazzo JP, Wang Z, Kinney JB, et al. (2015) Discovery of cancer drug targets by CRISPR-Cas9 screening of protein domains. Nat Biotechnol 33: 661-667. doi: 10.1038/nbt.3235PMID: 25961408
12. Moreno-Mateos MA, Vejnar CE, Beaudoin JD, Fernandez JP, Mis EK, et al. (2015) CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo. Nat Methods 12: 982-988. doi: 10.1038/nmeth.3543 PMID: 26322839
13. 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.
14. Daigle SR, Olhava EJ, Therkelsen CA, Basavapathruni A, Jin L, et al. (2013) Potent inhibition of DOT1L as treatment of MLL-fusion leukemia. Blood 122: 1017-1025. doi: 10.1182/blood-2013-04-497644PMID: 23801631
15. Knutson SK, Warholic NM, Wigle TJ, Klaus CR, Allain CJ, et al. (2013) Durable tumor regression in genetically altered malignant rhabdoid tumors by inhibition of methyltransferase EZH2. Proc Natl Acad Sci U S A 110: 7922-7927. doi: 10.1073/pnas.1303800110 PMID: 23620515
16. Hohmann AF, Martin LJ, Minder JL, Roe JS, Shi J, et al. (2016) Sensitivity and engineered resistance of myeloid leukemia cells to BRD9 inhibition. Nat Chem Biol.
17. Zuber J, McJunkin K, Fellmann C, Dow LE, Taylor MJ, et al. (2011) Toolkit for evaluating genes required for proliferation and survival using tetracycline-regulated RNAi. Nat Biotechnol 29: 79-83. doi: 10.1038/ nbt.1720 PMID: 21131983
18. Morita S, Kojima T, Kitamura T (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 7: 1063-1066. doi: 10.1038/sj.gt.3301206 PMID: 10871756
19. Nguyen AT, Zhang Y (2011) The diverse functions of Dot1 and H3K79 methylation. Genes Dev 25: 1345-1358. doi: 10.1101/gad.2057811 PMID: 21724828
20. Bernt KM, Zhu N, Sinha AU, Vempati S, Faber J, et al. (2011) MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 20: 66-78. doi: 10.1016/j.ccr.2011.06.010PMID: 21741597
21. Daigle SR, Olhava EJ, Therkelsen CA, Majer CR, Sneeringer CJ, et al. (2011) Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell 20: 53-65. doi: 10. 1016/j.ccr.2011.06.009 PMID: 21741596
22. 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: 633-646. doi: 10.1016/j. molcel.2016.06.037 PMID: 27499295
23. Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349. doi: 10.1038/nature09784 PMID: 21248841
24. Xu B, On DM, Ma A, Parton T, Konze KD, et al. (2015) Selective inhibition of EZH2 and EZH1 enzymatic activity by a small molecule suppresses MLL-rearranged leukemia. Blood 125: 346-357. doi: 10.1182/ blood-2014-06-581082 PMID: 25395428
25. Shi J, Wang E, Zuber J, Rappaport A, Taylor M, et al. (2013) The Polycomb complex PRC2 supports aberrant self-renewal in a mouse model of MLL-AF9;Nras(G12D) acute myeloid leukemia. Oncogene 32: 930-938. doi: 10.1038/onc.2012.110 PMID: 22469984
26. Neff T, Sinha AU, Kluk MJ, Zhu N, Khattab MH, et al. (2012) Polycomb repressive complex 2 is required for MLL-AF9 leukemia. Proc Natl Acad Sci U S A 109: 5028-5033. doi: 10.1073/pnas.1202258109PMID: 22396593
27. Chen SH, Zhang Y, Van Horn RD, Yin T, Buchanan S, et al. (2016) Oncogenic BRAF Deletions That Function as Homodimers and Are Sensitive to Inhibition by RAF Dimer Inhibitor LY3009120. Cancer Discov 6: 300-315. doi: 10.1158/2159-8290.CD-15-0896 PMID: 26732095
28. Donovan KF, Hegde M, Sullender M, Vaimberg EW, Johannessen CM, et al. (2017) Creation of Novel Protein Variants with CRISPR/Cas9-Mediated Mutagenesis: Turning a Screening By-Product into a Discovery Tool. PLoS One 12: e0170445. doi: 10.1371/journal.pone.0170445 PMID: 28118392
29. 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: 10.1038/nature17946PMID: 27096365
30. 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.
31. 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: 1036-1042. doi: 10.1038/nmeth.4038 PMID: 27798611
32. Ma Y, Zhang J, Yin W, Zhang Z, Song Y, et al. (2016) Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat Methods 13: 1029-1035. doi: 10. 1038/nmeth.4027 PMID: 27723754