Inhibition of CRISPR-Cas9 with Bacteriophage Proteins

Cell

Volumn 168, Issue 1-2, 2017, Pages 150-158.e10

  Rauch, Benjamin J ^a,b   Silvis, Melanie R ^a,c   Hultquist, Judd F ^b,c,d   Waters, Christopher S ^a,b,c   McGregor, Michael J ^b,c,d   Krogan, Nevan J ^b,c,d   Bondy Denomy, Joseph ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GLADSTONE INSTITUTES   (United States)

Author keywords

anti CRISPR; bacteriophage; Cas9; Cas9 inhibitor; CRISPR Cas; dCas9; gene editing; Listeria monocytogenes; prophage

Indexed keywords

BACTERIAL PROTEIN; CRISPR ASSOCIATED PROTEIN; INHIBITOR PROTEIN; CAS9 ENDONUCLEASE STREPTOCOCCUS PYOGENES; ENDONUCLEASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BACTERIOPHAGE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CODON; CONTROLLED STUDY; CRISPR CAS SYSTEM; ESCHERICHIA COLI; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INHIBITION KINETICS; LISTERIA MONOCYTOGENES; NONHUMAN; OPERON; PRIORITY JOURNAL; PROPHAGE; REPORTER GENE; STREPTOCOCCUS PYOGENES; VIRUS CELL TRANSFORMATION; ANTAGONISTS AND INHIBITORS; ENZYMOLOGY; GENETIC ENGINEERING; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; VIROLOGY;

BACTERIAL PROTEINS; BACTERIOPHAGES; CRISPR-CAS SYSTEMS; ENDONUCLEASES; ESCHERICHIA COLI; GENETIC ENGINEERING; HEK293 CELLS; HUMANS; LISTERIA MONOCYTOGENES; PROPHAGES;

EID: 85009201750     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.12.009     Document Type: Article

References (50)

1. Abudayyeh, O.O., Gootenberg, J.S., Konermann, S., Joung, J., Slaymaker, I.M., Cox, D.B.T., Shmakov, S., Makarova, K.S., Semenova, E., Minakhin, L., et al. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science, 353, 2016, aaf5573.
2. Barrangou, R., Doudna, J.A., Applications of CRISPR technologies in research and beyond. Nat. Biotechnol. 34 (2016), 933–941.
3. Biswas, A., Gagnon, J.N., Brouns, S.J.J., Fineran, P.C., Brown, C.M., CRISPRTarget: bioinformatic prediction and analysis of crRNA targets. RNA Biol. 10 (2013), 817–827.
4. Biswas, A., Staals, R.H.J., Morales, S.E., Fineran, P.C., Brown, C.M., CRISPRDetect: a flexible algorithm to define CRISPR arrays. BMC Genomics, 17, 2016, 356.
5. 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.
6. 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.
7. Brouns, S.J.J., Jore, M.M., Lundgren, M., Westra, E.R., Slijkhuis, R.J.H., Snijders, A.P.L., Dickman, M.J., Makarova, K.S., Koonin, E.V., van der Oost, J., Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321 (2008), 960–964.
8. Camilli, A., Tilney, L.G., Portnoy, D.A., Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8 (1993), 143–157.
9. Choi, K.-H., Gaynor, J.B., White, K.G., Lopez, C., Bosio, C.M., Karkhoff-Schweizer, R.R., Schweizer, H.P., A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2 (2005), 443–448.
10. 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.
11. 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.
12. Di, H., Ye, L., Yan, H., Meng, H., Yamasak, S., Shi, L., Comparative analysis of CRISPR loci in different Listeria monocytogenes lineages. Biochem. Biophys. Res. Commun. 454 (2014), 399–403.
13. East-Seletsky, A., O'Connell, M.R., Knight, S.C., Burstein, D., Cate, J.H.D., Tjian, R., Doudna, J.A., Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature 538 (2016), 270–273.
14. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (2004), 1792–1797.
15. Edgar, R., Qimron, U., The Escherichia coli CRISPR system protects from λ lysogenization, lysogens, and prophage induction. J. Bacteriol. 192 (2010), 6291–6294.
16. Garneau, J.E., Dupuis, M.-È., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A.H., Moineau, S., The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468 (2010), 67–71.
17. Gilbert, L.A., Larson, M.H., Morsut, L., Liu, Z., Brar, G.A., Torres, S.E., Stern-Ginossar, N., Brandman, O., Whitehead, E.H., Doudna, J.A., et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154 (2013), 442–451.
18. Goldberg, G.W., Jiang, W., Bikard, D., Marraffini, L.A., Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514 (2014), 633–637.
19. Grissa, I., Vergnaud, G., Pourcel, C., CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 35 (2007), W52–W57.
20. Guzman, L.M., Belin, D., Carson, M.J., Beckwith, J., Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177 (1995), 4121–4130.
21. Haldimann, A., Wanner, B.L., Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J. Bacteriol. 183 (2001), 6384–6393.
22. Haurwitz, R.E., Jinek, M., Wiedenheft, B., Zhou, K., Doudna, J.A., Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329 (2010), 1355–1358.
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. 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.
25. Labrie, S.J., Samson, J.E., Moineau, S., Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8 (2010), 317–327.
26. Lauer, P., Chow, M.Y.N., Loessner, M.J., Portnoy, D.A., Calendar, R., Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J. Bacteriol. 184 (2002), 4177–4186.
27. Loessner, M.J., Busse, M., Bacteriophage typing of Listeria species. Appl. Environ. Microbiol. 56 (1990), 1912–1918.
28. Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S., Costa, F., Shah, S.A., Saunders, S.J., Barrangou, R., Brouns, S.J.J., Charpentier, E., Haft, D.H., et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13 (2015), 722–736.
29. 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.
30. Mandin, P., Repoila, F., Vergassola, M., Geissmann, T., Cossart, P., Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res. 35 (2007), 962–974.
31. Marraffini, L.A., CRISPR-Cas immunity in prokaryotes. Nature 526 (2015), 55–61.
32. Maxwell, K.L., Garcia, B., Bondy-Denomy, J., Bona, D., Hidalgo-Reyes, Y., Davidson, A.R., The solution structure of an anti-CRISPR protein. Nat. Commun., 7, 2016, 13134.
33. Mojica, F.J.M., Díez-Villaseñor, C., García-Martínez, J., Soria, E., Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60 (2005), 174–182.
34. Nuñez, J.K., Kranzusch, P.J., Noeske, J., Wright, A.V., Davies, C.W., Doudna, J.A., Cas1-Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nat. Struct. Mol. Biol. 21 (2014), 528–534.
35. Park, S.F., Stewart, G.S., High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94 (1990), 129–132.
36. Pawluk, A., Bondy-Denomy, J., Cheung, V.H.W., 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, e00896–e14.
37. 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.
38. Qi, L.S., Larson, M.H., Gilbert, L.A., Doudna, J.A., Weissman, J.S., Arkin, A.P., Lim, W.A., Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152 (2013), 1173–1183.
39. 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.
40. Samai, P., Pyenson, N., Jiang, W., Goldberg, G.W., Hatoum-Aslan, A., Marraffini, L.A., Co-transcriptional DNA and RNA cleavage during Type III CRISPR-Cas immunity. Cell 161 (2015), 1164–1174.
41. Samson, J.E., Magadán, A.H., Sabri, M., Moineau, S., Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11 (2013), 675–687.
42. Sesto, N., Touchon, M., Andrade, J.M., Kondo, J., Rocha, E.P.C., Arraiano, C.M., Archambaud, C., Westhof, É., Romby, P., Cossart, P., A PNPase dependent CRISPR system in Listeria. PLoS Genet., 10, 2014, e1004065.
43. Söding, J., Biegert, A., Lupas, A.N., The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33 (2005), W244–W248.
44. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30 (2013), 2725–2729.
45. Typas, A., Nichols, R.J., Siegele, D.A., Shales, M., Collins, S.R., Lim, B., Braberg, H., Yamamoto, N., Takeuchi, R., Wanner, B.L., et al. High-throughput, quantitative analyses of genetic interactions in E. coli. Nat. Methods 5 (2008), 781–787.
46. Wang, X., Yao, D., Xu, J.-G., Li, A.-R., Xu, J., Fu, P., Zhou, Y., Zhu, Y., Structural basis of Cas3 inhibition by the bacteriophage protein AcrF3. Nat. Struct. Mol. Biol. 23 (2016), 868–870.
47. Wright, A.V., Nuñez, J.K., Doudna, J.A., Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164 (2016), 29–44.
48. Yosef, I., Goren, M.G., Qimron, U., Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 40 (2012), 5569–5576.
49. Zemansky, J., Kline, B.C., Woodward, J.J., Leber, J.H., Marquis, H., Portnoy, D.A., Development of a mariner-based transposon and identification of Listeria monocytogenes determinants, including the peptidyl-prolyl isomerase PrsA2, that contribute to its hemolytic phenotype. J. Bacteriol. 191 (2009), 3950–3964.
50. Zetsche, B., Gootenberg, J.S., Abudayyeh, O.O., Slaymaker, I.M., Makarova, K.S., Essletzbichler, P., Volz, S.E., Joung, J., van der Oost, J., Regev, A., et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163 (2015), 759–771.