Naturally Occurring Off-Switches for CRISPR-Cas9

Cell

Volumn 167, Issue 7, 2016, Pages 1829-1838.e9

  Pawluk, April ^a   Amrani, Nadia ^b   Zhang, Yan ^b   Garcia, Bianca ^a   Hidalgo Reyes, Yurima ^a   Lee, Jooyoung ^b   Edraki, Alireza ^b   Shah, Megha ^a   Sontheimer, Erik J ^b   Maxwell, Karen L ^a   Davidson, Alan R ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

anti CRISPR; Cas9; CRISPR Cas; genome editing; Neisseria meningitidis; phage

Indexed keywords

ARTICLE; BACTERIAL GENOME; BIOINFORMATICS; CONTROLLED STUDY; CRISPR CAS SYSTEM; GENE ACTIVITY; GENE EDITING; GENE SWITCHING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; CELL LINE; GENETICS; METABOLISM;

BACTERIAL PROTEIN;

BACTERIAL PROTEINS; CELL LINE; CRISPR-CAS SYSTEMS; GENE EDITING; HUMANS; NEISSERIA MENINGITIDIS;

EID: 85006307718     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.11.017     Document Type: Article

References (66)

1. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A., Horvath, P., CRISPR provides acquired resistance against viruses in prokaryotes. Science 315 (2007), 1709–1712.
2. Bikard, D., Euler, C.W., Jiang, W., Nussenzweig, P.M., Goldberg, G.W., Duportet, X., Fischetti, V.A., Marraffini, L.A., Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat. Biotechnol. 32 (2014), 1146–1150.
3. Bolukbasi, M.F., Gupta, A., Wolfe, S.A., Creating and evaluating accurate CRISPR-Cas9 scalpels for genomic surgery. Nat. Methods 13 (2016), 41–50.
4. Bondy-Denomy, J., Pawluk, A., Maxwell, K.L., Davidson, A.R., Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493 (2013), 429–432.
5. Bondy-Denomy, J., Garcia, B., Strum, S., Du, M., Rollins, M.F., Hidalgo-Reyes, Y., Wiedenheft, B., Maxwell, K.L., Davidson, A.R., Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins. Nature 526 (2015), 136–139.
6. 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 (2013), 230–232.
7. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., Zhang, F., Multiplex genome engineering using CRISPR/Cas systems. Science 339 (2013), 819–823.
8. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J., Charpentier, E., CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471 (2011), 602–607.
9. 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 (2016), 5–15.
10. Duffin, P.M., Seifert, H.S., Genetic transformation of Neisseria gonorrhoeae shows a strand preference. FEMS Microbiol. Lett. 334 (2012), 44–48.
11. Ebina, H., Misawa, N., Kanemura, Y., Koyanagi, Y., Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus. Sci. Rep., 3, 2013, 2510.
12. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (2004), 1792–1797.
13. Esvelt, K.M., Mali, P., Braff, J.L., Moosburner, M., Yaung, S.J., Church, G.M., Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat. Methods 10 (2013), 1116–1121.
14. Fineran, P.C., Gerritzen, M.J., Suárez-Diez, M., Künne, T., Boekhorst, J., van Hijum, S.A., Staals, R.H., Brouns, S.J., Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl. Acad. Sci. USA 111 (2014), E1629–E1638.
15. Fonfara, I., Le Rhun, A., Chylinski, K., Makarova, K.S., Lécrivain, A.L., Bzdrenga, J., Koonin, E.V., Charpentier, E., Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res. 42 (2014), 2577–2590.
16. Fu, Y., Sander, J.D., Reyon, D., Cascio, V.M., Joung, J.K., Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32 (2014), 279–284.
17. Gantz, V.M., Jasinskiene, N., Tatarenkova, O., Fazekas, A., Macias, V.M., Bier, E., James, A.A., Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc. Natl. Acad. Sci. USA 112 (2015), E6736–E6743.
18. Gasiunas, G., Barrangou, R., Horvath, P., Siksnys, V., Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. USA 109 (2012), E2579–E2586.
19. Gomaa, A.A., Klumpe, H.E., Luo, M.L., Selle, K., Barrangou, R., Beisel, C.L., Programmable removal of bacterial strains by use of genome-targeting CRISPR-Cas systems. MBio, 5, 2014 e00928–13.
20. Gophna, U., Kristensen, D.M., Wolf, Y.I., Popa, O., Drevet, C., Koonin, E.V., No evidence of inhibition of horizontal gene transfer by CRISPR-Cas on evolutionary timescales. ISME J. 9 (2015), 2021–2027.
21. Guschin, D.Y., Waite, A.J., Katibah, G.E., Miller, J.C., Holmes, M.C., Rebar, E.J., A rapid and general assay for monitoring endogenous gene modification. Methods Mol. Biol. 649 (2010), 247–256.
22. Hammond, A., Galizi, R., Kyrou, K., Simoni, A., Siniscalchi, C., Katsanos, D., Gribble, M., Baker, D., Marois, E., Russell, S., et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat. Biotechnol. 34 (2016), 78–83.
23. Heler, R., Samai, P., Modell, J.W., Weiner, C., Goldberg, G.W., Bikard, D., Marraffini, L.A., Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature 519 (2015), 199–202.
24. Hilton, I.B., D'Ippolito, A.M., Vockley, C.M., Thakore, P.I., Crawford, G.E., Reddy, T.E., Gersbach, C.A., Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33 (2015), 510–517.
25. Hirano, H., Gootenberg, J.S., Horii, T., Abudayyeh, O.O., Kimura, M., Hsu, P.D., Nakane, T., Ishitani, R., Hatada, I., Zhang, F., et al. Structure and engineering of Francisella novicida Cas9. Cell 164 (2016), 950–961.
26. Hou, Z., Zhang, Y., Propson, N.E., Howden, S.E., Chu, L.F., Sontheimer, E.J., Thomson, J.A., Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 110 (2013), 15644–15649.
27. Hsu, P.D., Scott, D.A., Weinstein, J.A., Ran, F.A., Konermann, S., Agarwala, V., Li, Y., Fine, E.J., Wu, X., Shalem, O., et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31 (2013), 827–832.
28. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Kaini, P., Sander, J.D., Joung, J.K., Peterson, R.T., Yeh, J.R., Heritable and precise zebrafish genome editing using a CRISPR-Cas system. PLoS ONE, 8, 2013, e68708.
29. Jiang, W., Bikard, D., Cox, D., Zhang, F., Marraffini, L.A., RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31 (2013), 233–239.
30. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821.
31. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E., Doudna, J., RNA-programmed genome editing in human cells. eLife, 2, 2013, e00471.
32. Jinek, M., Jiang, F., Taylor, D.W., Sternberg, S.H., Kaya, E., Ma, E., Anders, C., Hauer, M., Zhou, K., Lin, S., et al. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science, 343, 2014, 1247997.
33. Kaminski, R., Chen, Y., Fischer, T., Tedaldi, E., Napoli, A., Zhang, Y., Karn, J., Hu, W., Khalili, K., Elimination of HIV-1 genomes from human t-lymphoid cells by CRISPR/Cas9 Gene Editing. Sci. Rep., 6, 2016, 22555.
34. Kearns, N.A., Genga, R.M., Enuameh, M.S., Garber, M., Wolfe, S.A., Maehr, R., Cas9 effector-mediated regulation of transcription and differentiation in human pluripotent stem cells. Development 141 (2014), 219–223.
35. Kearns, N.A., Pham, H., Tabak, B., Genga, R.M., Silverstein, N.J., Garber, M., Maehr, R., Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat. Methods 12 (2015), 401–403.
36. Lee, C.M., Cradick, T.J., Bao, G., The Neisseria meningitidis CRISPR-Cas9 System Enables Specific Genome Editing in Mammalian Cells. Mol. Ther. 24 (2016), 645–654.
37. Ma, E., Harrington, L.B., O'Connell, M.R., Zhou, K., Doudna, J.A., Single-stranded DNA cleavage by divergent CRISPR-Cas9 enzymes. Mol. Cell 60 (2015), 398–407.
38. Ma, H., Naseri, A., Reyes-Gutierrez, P., Wolfe, S.A., Zhang, S., Pederson, T., Multicolor CRISPR labeling of chromosomal loci in human cells. Proc. Natl. Acad. Sci. USA 112 (2015), 3002–3007.
39. Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S., Costa, F., Shah, S.A., Saunders, S.J., Barrangou, R., Brouns, S.J., Charpentier, E., Haft, D.H., et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13 (2015), 722–736.
40. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., Church, G.M., RNA-guided human genome engineering via Cas9. Science 339 (2013), 823–826.
41. Müller, M., Lee, C.M., Gasiunas, G., Davis, T.H., Cradick, T.J., Siksnys, V., Bao, G., Cathomen, T., Mussolino, C., Streptococcus thermophilus CRISPR-Cas9 systems enable specific editing of the human genome. Mol. Ther. 24 (2016), 636–644.
42. Nihongaki, Y., Kawano, F., Nakajima, T., Sato, M., Photoactivatable CRISPR-Cas9 for optogenetic genome editing. Nat. Biotechnol. 33 (2015), 755–760.
43. Nuñez, J.K., Harrington, L.B., Doudna, J.A., Chemical and biophysical modulation of Cas9 for tunable genome engineering. ACS Chem. Biol. 11 (2016), 681–688.
44. Orthwein, A., Noordermeer, S.M., Wilson, M.D., Landry, S., Enchev, R.I., Sherker, A., Munro, M., Pinder, J., Salsman, J., Dellaire, G., et al. A mechanism for the suppression of homologous recombination in G1 cells. Nature 528 (2015), 422–426.
45. Ousterout, D.G., Kabadi, A.M., Thakore, P.I., Majoros, W.H., Reddy, T.E., Gersbach, C.A., Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat. Commun., 6, 2015, 6244.
46. Pattanayak, V., Lin, S., Guilinger, J.P., Ma, E., Doudna, J.A., Liu, D.R., High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31 (2013), 839–843.
47. Pawluk, A., Bondy-Denomy, J., Cheung, V.H., Maxwell, K.L., Davidson, A.R., A new group of phage anti-CRISPR genes inhibits the type I-E CRISPR-Cas system of Pseudomonas aeruginosa. MBio, 5, 2014, e00896.
48. Pawluk, A., Staals, R.H.J., Taylor, C., Watson, B.N.J., Saha, S., Fineran, P.C., Maxwell, K.L., Davidson, A.R., Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat. Microbiol., 1, 2016, 16085.
49. Peränen, J., Rikkonen, M., Hyvönen, M., Kääriäinen, L., T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli. Anal. Biochem. 236 (1996), 371–373.
50. Price, M.N., Dehal, P.S., Arkin, A.P., FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26 (2009), 1641–1650.
51. Price, M.N., Dehal, P.S., Arkin, A.P., FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE, 5, 2010, e9490.
52. Ran, F.A., Cong, L., Yan, W.X., Scott, D.A., Gootenberg, J.S., Kriz, A.J., Zetsche, B., Shalem, O., Wu, X., Makarova, K.S., et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 520 (2015), 186–191.
53. Richter, C., Dy, R.L., McKenzie, R.E., Watson, B.N., Taylor, C., Chang, J.T., McNeil, M.B., Staals, R.H., Fineran, P.C., Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer. Nucleic Acids Res. 42 (2014), 8516–8526.
54. Takeuchi, N., Wolf, Y.I., Makarova, K.S., Koonin, E.V., Nature and intensity of selection pressure on CRISPR-associated genes. J. Bacteriol. 194 (2012), 1216–1225.
55. Touchon, M., Bernheim, A., Rocha, E.P., Genetic and life-history traits associated with the distribution of prophages in bacteria. ISME J. 10 (2016), 2744–2754.
56. van Houte, S., Ekroth, A.K., Broniewski, J.M., Chabas, H., Ashby, B., Bondy-Denomy, J., Gandon, S., Boots, M., Paterson, S., Buckling, A., Westra, E.R., The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 532 (2016), 385–388.
57. Villefranc, J.A., Amigo, J., Lawson, N.D., Gateway compatible vectors for analysis of gene function in the zebrafish. Dev. Dyn. 236 (2007), 3077–3087.
58. Wang, H., Yang, H., Shivalila, C.S., Dawlaty, M.M., Cheng, A.W., Zhang, F., Jaenisch, R., One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153 (2013), 910–918.
59. Wang, H., La Russa, M., Qi, L.S., CRISPR/Cas9 in genome editing and beyond. Annu. Rev. Biochem. 85 (2016), 227–264.
60. Wei, Y., Terns, R.M., Terns, M.P., Cas9 function and host genome sampling in Type II-A CRISPR-Cas adaptation. Genes Dev. 29 (2015), 356–361.
61. Wright, A.V., Sternberg, S.H., Taylor, D.W., Staahl, B.T., Bardales, J.A., Kornfeld, J.E., Doudna, J.A., Rational design of a split-Cas9 enzyme complex. Proc. Natl. Acad. Sci. USA 112 (2015), 2984–2989.
62. Wu, Y., Liang, D., Wang, Y., Bai, M., Tang, W., Bao, S., Yan, Z., Li, D., Li, J., Correction of a genetic disease in mouse via use of CRISPR-Cas9. Cell Stem Cell 13 (2013), 659–662.
63. Yen, S.T., Zhang, M., Deng, J.M., Usman, S.J., Smith, C.N., Parker-Thornburg, J., Swinton, P.G., Martin, J.F., Behringer, R.R., Somatic mosaicism and allele complexity induced by CRISPR/Cas9 RNA injections in mouse zygotes. Dev. Biol. 393 (2014), 3–9.
64. Yin, H., Xue, W., Chen, S., Bogorad, R.L., Benedetti, E., Grompe, M., Koteliansky, V., Sharp, P.A., Jacks, T., Anderson, D.G., Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat. Biotechnol. 32 (2014), 551–553.
65. Zhang, Y., Heidrich, N., Ampattu, B.J., Gunderson, C.W., Seifert, H.S., Schoen, C., Vogel, J., Sontheimer, E.J., Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol. Cell 50 (2013), 488–503.
66. Zhang, Y., Rajan, R., Seifert, H.S., Mondragón, A., Sontheimer, E.J., DNase H activity of Neisseria meningitidis Cas9. Mol. Cell 60 (2015), 242–255.