RNA-guided transcriptional silencing in vivo with S. aureus CRISPR-Cas9 repressors

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Thakore, Pratiksha I ^a,b   Kwon, Jennifer B ^b,c   Nelson, Christopher E ^a,b   Rouse, Douglas C ^d   Gemberling, Matthew P ^a,b   Oliver, Matthew L ^a   Gersbach, Charles A ^a,b,c  

^a USA   (United States)

^b DUKE UNIVERSITY   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; ALANINE AMINOTRANSFERASE; CHOLESTEROL; GUIDE RNA; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PROPROTEIN CONVERTASE 9; BACTERIAL PROTEIN; ENDONUCLEASE; PCSK9 PROTEIN, MOUSE;

BACTERIUM; GENE EXPRESSION; GENETIC ENGINEERING; PHENOTYPE; RESEARCH METHOD; RNA; SERUM;

ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; AML12 CELL LINE; ANIMAL CELL; ARTICLE; BASIC RESEARCH; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CRISPR-CAS9 SYSTEM; FAMILIAL HYPERCHOLESTEROLEMIA; GENE CONTROL; GENE EDITING; GENE SILENCING; HEK293T CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LIVER; MALE; MOUSE; NONHUMAN; PHENOTYPE; RNA SEQUENCE; STAPHYLOCOCCUS AUREUS; WILD TYPE MOUSE; ANIMAL; BLOOD; C57BL MOUSE; CRISPR CAS SYSTEM; ENZYMOLOGY; GENE THERAPY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

ANIMALIA; MUS; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL PROTEINS; CHOLESTEROL; CRISPR-CAS SYSTEMS; ENDONUCLEASES; GENE SILENCING; GENETIC THERAPY; LIVER; MALE; MICE; MICE, INBRED C57BL; PROPROTEIN CONVERTASE 9; RNA, GUIDE; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION, GENETIC;

EID: 85045986372     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-04048-4     Document Type: Article

References (52)

1. Thakore, P. I., Black, J. B., Hilton, I. B. & Gersbach, C. A. Editing the epigenome: technologies for programmable transcription and epigenetic modulation. Nat. Methods 13, 127-137 (2016).
2. Dominguez, A. A., Lim, W. A. & Qi, L. S. Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation. Nat. Rev. Mol. Cell Biol. 17, 5-15 (2016).
3. Qi, L. S. et al. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152, 1173-1183 (2013).
4. Gilbert, L. A. et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154, 442-451 (2013).
5. Gilbert, L. A. et al. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159, 647-661 (2014).
6. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
7. Perez-Pinera, P. et al. RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat. Methods 10, 973-976 (2013).
8. Maeder, M. L. et al. CRISPR RNA-guided activation of endogenous human genes. Nat. Methods 10, 977-979 (2013).
9. Konermann, S. et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517, 583-588 (2015).
10. Chavez, A. et al. Highly efficient Cas9-mediated transcriptional programming. Nat. Methods 12, 326-328 (2015).
11. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
12. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
13. Kearns, N. A. et al. Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat. Methods 12, 401-403 (2015).
14. Gao, X. et al. Comparison of TALE designer transcription factors and the CRISPR/dCas9 in regulation of gene expression by targeting enhancers. Nucleic Acids Res. 42, e155 (2014).
15. Thakore, P. I. et al. Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nat. Methods 12, 1143-1149 (2015).
16. MaederM. L. & GersbachC. A. Genome editing technologies for gene and cell therapy. Mol. Ther. 24, 430-446 (2016).
17. Nelson, C. E. & Gersbach, C. A. Engineering delivery vehicles for genome editing. Annu Rev. Chem. Biomol. Eng. 7, 637-662 (2016).
18. Braun, C. J. et al. Versatile in vivo regulation of tumor phenotypes by dCas9-mediated transcriptional perturbation. Proc. Natl. Acad. Sci. USA 113, E3892-E3900 (2016).
19. Zheng, Y. et al. CRISPR interference-based specific and efficient gene inactivation in the brain. Nat. Neurosci. 21, 447-454 (2018).
20. Asokan, A., Schaffer, D. V. & Samulski, R. J. The AAV vector toolkit: poised at the clinical crossroads. Mol. Ther. 20, 699-708 (2012).
21. Gaj, T., Epstein, B. E. & Schaffer, D. V. Genome engineering using adeno-associated virus: basic and clinical research applications. Mol. Ther. 24, 458-464 (2016).
22. Swiech, L. et al. In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat. Biotechnol. 33, 102-106 (2015).
23. Long, C. et al. Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351, 400-403 (2016).
24. Suzuki, K. et al. In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration. Nature 540, 144-149 (2016).
25. Dong, B., Nakai, H. & Xiao, W. Characterization of genome integrity for oversized recombinant AAV vector. Mol. Ther. 18, 87-92 (2010).
26. Wu, Z., Yang, H. & Colosi, P. Effect of genome size on AAV vector packaging. Mol. Ther. 18, 80-86 (2010).
27. Ran, F. A. et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520, 186-191 (2015).
28. Nelson, C. E. et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351, 403-407 (2016).
29. Tabebordbar, M. et al. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351, 407-411 (2016).
30. Abifadel, M. et al. Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat. Genet. 34, 154-156 (2003).
31. Maxwell, K. N. & Breslow, J. L. Adenoviral-mediated expression of Pcsk9 in mice results in a low-density lipoprotein receptor knockout phenotype. Proc. Natl. Acad. Sci. USA 101, 7100-7105 (2004).
32. Cohen, J. C., Boerwinkle, E., Mosley, T. H. Jr. & Hobbs, H. H. Sequence variations in PCSK9, low LDL, and protection against coronary heart disease. N. Engl. J. Med. 354, 1264-1272 (2006).
33. He, N. Y. et al. Lowering serum lipids via PCSK9-targeting drugs: current advances and future perspectives. Acta Pharmacol. Sin. 38, 301-311 (2017).
34. Ridker, P. M. et al. Cardiovascular efficacy and safety of bococizumab in high-risk patients. N. Engl. J. Med. 376, 1527-1539 (2017).
35. Sabatine, M. S. et al. Evolocumab and clinical outcomes in patients with cardiovascular disease. N. Engl. J. Med. 376, 1713-1722 (2017).
36. Fitzgerald, K. et al. A highly durable RNAi therapeutic inhibitor of PCSK9. N. Engl. J. Med. 376, 41-51 (2017).
37. Ding, Q. et al. Permanent alteration of PCSK9 with in vivo CRISPR-Cas9 genome editing. Circ. Res. 115, 488-492 (2014).
38. Yue, F. et al. A comparative encyclopedia of DNA elements in the mouse genome. Nature 515, 355-364 (2014).
39. Bae, S., Park, J. & Kim, J. S. Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases. Bioinformatics 30, 1473-1475 (2014).
40. Gorski, S. A., Vogel, J. & Doudna, J. A. RNA-based recognition and targeting: sowing the seeds of specificity. Nat. Rev. Mol. Cell Biol. 18, 215-228 (2017).
41. Chew, W. L. et al. A multifunctional AAV-CRISPR-Cas9 and its host response. Nat. Methods 13, 868-874 (2016).
42. Manno, C. S. et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12, 342-347 (2006).
43. George, L. A. et al. Hemophilia B gene therapy with a high-specific-activity Factor IX variant. N. Engl. J. Med. 377, 2215-2227 (2017).
44. Liao, H. K. et al. In vivo target gene activation via CRISPR/Cas9-mediated trans-epigenetic modulation. Cell 171, 1495-1507 e1415 (2017).
45. Amabile, A. et al. Inheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing. Cell 167, 219-232 e214 (2016).
46. Ran, F. A. et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520, 186-191 (2015).
47. Salmon, P. & Trono, D. Production and titration of lentiviral vectors. Curr. Protoc. Neurosci. 5, 4.21.1-4.21.23 (2006).
48. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
49. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
50. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550 (2005).
51. Quinlan, A. R. BEDTools: the Swiss-army tool for genome feature analysis. Curr. Protoc. Bioinform. 47, 11.12.1-11.12.34 (2014).
52. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).