Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases

Nature Biotechnology

Volumn 33, Issue 2, 2015, Pages 179-188

  Frock, Richard L ^a,b,c   Hu, Jiazhi ^a,b,c   Meyers, Robin M ^a,b,c   Ho, Yu Jui ^a,b,c   Kii, Erina ^a,b,c   Alt, Frederick W ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DAMAGE DETECTION; GENE ENCODING;

CLEAVAGE EVENTS; COLLATERAL DAMAGE; COLLATERAL EFFECTS; HIGH THROUGHPUT; HOMOLOGOUS CHROMOSOMES; HOT SPOT; HUMAN GENOMES; LINEAR AMPLIFICATION;

GENES;

NUCLEASE; DNA; ENDONUCLEASE; GUIDE RNA; HOMEODOMAIN PROTEIN; RAG-1 PROTEIN;

ARTICLE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; ENZYME ENGINEERING; GENE AMPLIFICATION; GENE SEQUENCE; GENE TRANSLOCATION; GENOME; HUMAN; PRIORITY JOURNAL; BIOSYNTHESIS; CRISPR CAS SYSTEM; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN GENOME; PROTEIN ENGINEERING; RNA EDITING;

CRISPR-CAS SYSTEMS; DNA; DNA BREAKS, DOUBLE-STRANDED; ENDONUCLEASES; GENOME, HUMAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMEODOMAIN PROTEINS; HUMANS; PROTEIN ENGINEERING; RNA EDITING; RNA, GUIDE;

EID: 84923275611     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.3101     Document Type: Article

References (46)

1. Sander, J.D. & Joung, J.K. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347-355 (2014).
2. Kim, H. & Kim, J.S. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 15, 321-334 (2014).
3. 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).
4. Yin, H. et al. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat. Biotechnol. 32, 551-553 (2014).
5. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
6. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
7. Jinek, M. et al. RNA-programmed genome editing in human cells. eLife 2, e00471 (2013).
8. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
9. Christian, M. et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757-761 (2010).
10. Miller, J.C. et al. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148 (2011).
11. Mussolino, C. et al. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res. 39, 9283-9293 (2011).
12. Hsu, P.D. et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832 (2013).
13. Doyle, E.L. et al. TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res. 40, W117-122 (2012).
14. Xiao, A. et al. CasOT: a genome-wide Cas9/sgRNA off-target searching tool. Bioinformatics 30, 1180-1182 (2014).
15. Fu, Y. et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826 (2013).
16. Pattanayak, V. et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843 (2013).
17. Gabriel, R. et al. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat. Biotechnol. 29, 816-823 (2011).
18. Petek, L.M., Russell, D.W. & Miller, D.G. Frequent endonuclease cleavage at off-target locations in vivo. Mol. Ther. 18, 983-986 (2010).
19. Wood, A.J. et al. Targeted genome editing across species using ZFNs and TALENs. Science 333, 307 (2011).
20. Sung, Y.H. et al. Knockout mice created by TALEN-mediated gene targeting. Nat. Biotechnol. 31, 23-24 (2013).
21. Mitelman, F., Johansson, B. & Mertens, F. The impact of translocations and gene fusions on cancer causation. Nat. Rev. Cancer 7, 233-245 (2007).
22. Stephens, P.J. et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 462, 1005-1010 (2009).
23. Chiarle, R. et al. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147, 107-119 (2011).
24. Klein, I.A. et al. Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 147, 95-106 (2011).
25. Hu, J., Tepsuporn, S., Meyers, R.M., Gostissa, M. & Alt, F.W. Developmental propagation of V(D)J recombination-associated DNA breaks and translocations in mature B cells via dicentric chromosomes. Proc. Natl. Acad. Sci. USA 111, 10269-10274 (2014).
26. Barlow, J.H. et al. Identification of early replicating fragile sites that contribute to genome instability. Cell 152, 620-632 (2013).
27. Zhang, Y. et al. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148, 908-921 (2012).
28. Schmidt, M. et al. High-resolution insertion-site analysis by linear amplification-mediated PCR (LAM-PCR). Nat. Methods 4, 1051-1057 (2007).
29. Lee, Y.N. et al. A systematic analysis of recombination activity and genotype-phenotype correlation in human recombination-activating gene 1 deficiency. J. Allergy Clin. Immunol. 133, 1099-1108 (2014).
30. Muñoz, I.G. et al. Molecular basis of engineered meganuclease targeting of the endogenous human RAG1 locus. Nucleic Acids Res. 39, 729-743 (2011).
31. Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).
32. Hakim, O. et al. DNA damage defines sites of recurrent chromosomal translocations in B lymphocytes. Nature 484, 69-74 (2012).
33. Alt, F.W., Zhang, Y., Meng, F.L., Guo, C. & Schwer, B. Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 152, 417-429 (2013).
34. Gostissa, M. et al. IgH class switching exploits a general property of two DNA breaks to be joined in cis over long chromosomal distances. Proc. Natl. Acad. Sci. USA 111, 2644-2649 (2014).
35. Mali, P. et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833-838 (2013).
36. Ran, F.A. et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013).
37. Reyon, D. et al. FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 30, 460-465 (2012).
38. Jiang, W., Bikard, D., Cox, D., Zhang, F. & Marraffini, L.A. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31, 233-239 (2013).
39. Asaithamby, A. & Chen, D.J. Cellular responses to DNA double-strand breaks after low-dose gamma-irradiation. Nucleic Acids Res. 37, 3912-3923 (2009).
40. Franco, S. et al. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol. Cell 21, 201-214 (2006).
41. Ramiro, A.R. et al. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 440, 105-109 (2006).
42. Hastings, P.J., Lupski, J.R., Rosenberg, S.M. & Ira, G. Mechanisms of change in gene copy number. Nat. Rev. Genet. 10, 551-564 (2009).
43. Guilinger, J.P. et al. Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity. Nat. Methods 11, 429-435 (2014).
44. Zhou, Z.X. et al. Mapping genomic hotspots of DNA damage by a single-strand-DNA-compatible and strand-specific ChIP-seq method. Genome Res. 23, 705-715 (2013).
45. Faust, G.G. & Hall, I.M. YAHA: fast and flexible long-read alignment with optimal breakpoint detection. Bioinformatics 28, 2417-2424 (2012).
46. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).