Kinetics of the CRISPR-Cas9 effector complex assembly and the role of 3′-terminal segment of guide RNA

Nucleic Acids Research

Volumn 44, Issue 6, 2016, Pages 2837-2845

  Mekler, Vladimir ^a   Minakhin, Leonid ^a   Semenova, Ekaterina ^a   Kuznedelov, Konstantin ^a   Severinov, Konstantin ^a,b,c  

^a RUTGERS UNIVERSITY   (United States)

^b INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

^c PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CAS9 PROTEIN; CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; CRISPR ASSOCIATED PROTEIN; RNA; SINGLE GUIDE RNA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CAS9 ENDONUCLEASE STREPTOCOCCUS PYOGENES; ENDONUCLEASE; GUIDE RNA; OLIGONUCLEOTIDE; PROTEIN BINDING;

3' UNTRANSLATED REGION; ARTICLE; BINDING KINETICS; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); FLUORESCENCE RESONANCE ENERGY TRANSFER; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA SYNTHESIS; BASE PAIRING; BINDING COMPETITION; BINDING SITE; BIOASSAY; CHEMISTRY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; STREPTOCOCCUS PYOGENES; SYNTHESIS;

BACTERIAL PROTEINS; BASE PAIRING; BASE SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; BIOLOGICAL ASSAY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; ENDONUCLEASES; FLUORESCENCE RESONANCE ENERGY TRANSFER; KINETICS; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES; PROTEIN BINDING; RNA, GUIDE; STREPTOCOCCUS PYOGENES;

EID: 84963831923     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw138     Document Type: Article

References (45)

1. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A. and Horvath, P. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315, 1709-1712.
2. Brouns, S.J., Jore, M.M., Lundgren, M., Westra, E.R., Slijkhuis, R.J., Snijders, A.P., Dickman, M.J., Makarova, K.S., Koonin, E.V. and van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321, 960-964.
3. Garneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A.H. and Moineau, S. (2011) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468, 67-71.
4. Jore, M.M., Lundgren, M., Van Duijn, E., Bultema, J.B., Westra, E.R., Waghmare, S.P., Wiedenheft, B., Pul, U., Wurm, R., Wagner, R. et al. (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol., 18, 529-536.
5. Szczelkun, M.D., Tikhomirova, M.S., Sinkunas, T., Gasiunas, G., Karvelis, T., Pschera, P., Siksnys, V. and Seidel, R. (2014) Direct observation of R-loop formation by single RNA-guided Cas9 and Cascade effector complexes. Proc. Natl. Acad. Sci. U.S.A., 111, 9798-9803.
6. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J. and Charpentier, E. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 471, 602-607.
7. Sapranauskas, R., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P. and Siksnys, V. (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res., 39, 9275-9282.
8. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A. and Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
9. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A. et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
10. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T, Yeh, J.R. and Joung, J.K. (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol., 31, 227-229.
11. Sander, J.D. and Joung, J.K. (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol., 32, 347-55.
12. 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. (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154, 442-451.
13. Chen, B., Gilbert, L.A., Cimini, B.A., Schnitzbauer, J., Zhang, W., Li, G.W., Park, J., Blackburn, E.H., Weissman, J.S., Qi, L.S. et al. (2013) Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 155, 1479-1491.
14. 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. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol., 31, 827-832.
15. Fu, Y., Sander, J.D., Reyon, D., Cascio, V.M. and Joung, J.K. (2014) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol., 32, 279-284.
16. Doench, J.G., Hartenian, E., Graham, D.B., Tothova, Z., Hegde, M., Smith, I., Sullender, M., Ebert, B.L., Xavier, R.J. and Root, D.E. (2014) Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol., 32, 1262-1267.
17. Josephs, E.A., Kocak, D.D., Fitzgibbon, C.J., McMenemy, J., Gersbach, C.A. and Marszalek, P.E. (2015) Structure and specificity of the RNA-guided endonuclease Cas9 during DNA interrogation, target binding and cleavage. Nucleic Acids Res., 43, 8924-8941.
18. Moreno-Mateos, M.A., Vejnar, C.E., Beaudoin, J.D., Fernandez, J.P., Mis, E.K., Khokha, M.K. and Giraldez, A.J. (2015) CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo. Nat. Methods 12, 982-988.
19. Ran, F., Hsu, P.D., Lin, C.-Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., Scott, D.A., Inoue, A., Matoba, S. and Zhang, Y. (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 154, 1380-1389.
20. Mali, P., Aach, J., Stranges, P.B., Esvelt, K.M., Moosburner, M., Kosuri, S., Yang, L. and Church, G.M. (2013) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol., 31, 833-838.
21. Tsai, S.Q., Wyvekens, N., Khayter, C., Foden, J.A., Thapar, V., Reyon, D., Goodwin, M. J., Aryee, M.J. and Joung, J.K. (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol., 32, 569-576.
22. Guilinger, J.P., Thompson, D.B. and Liu, D.R. (2014) Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat. Biotechnol., 32, 577-582.
23. Davis, K.M, Pattanayak, V., Thompson, D.B., Zuris, J.A. and Liu, D.R. (2015) Small molecule-triggered Cas9 protein with improved genome-editing specificity. Nat. Chem. Biol., 11, 316-318.
24. Wright, A.V., Sternberg, S.H., Taylor, D.W., Staahl, B.T., Bardales, J.A., Kornfeld, J.E. and Doudna, J.A. (2015) Rational design of a split-Cas9 enzyme complex. Proc. Natl. Acad. Sci. U.S.A., 112, 2984-2989.
25. Slaymaker, I.M., Gao, L., Zetsche, B., Scott, D.A., Yan, W.X. and Zhang, F. (2016) Rationally engineered Cas9 nucleases with improved specificity. Science, 351, 84-88.
26. Nishimasu, H., Ran, F.A., Hsu, P.D., Konermann, S., Shehata, S.I., Dohmae, N., Ishitani, R., Zhang, F. and Nureki, O. (2014) Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell, 156, 935-949.
27. Briner, A., Donohoue, P., Gomaa, A., Selle, K., Slorach, E., Nye, C., Haurwitz, R., Beisel, C., May, A. and Barrangou, R. (2014) Guide RNA functional modules direct Cas9 activity and orthogonality. Mol. Cell, 56, 333-339.
28. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E. and Doudna, J. (2013) RNA-programmed genome editing in human cells. Elife, 2, 1-9.
29. Zhou, H., Liu, B., Weeks, D.P., Spalding, M.H. and Yang, B. (2014) Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res., 42, 10903-10914.
30. Wu, X., Scott, D.A., Kriz, A.J., Chiu, A.C., Hsu, P.D., Dadon, D.B., Cheng, A.W., Trevino, A.E., Konermann, S., Chen, S. et al. (2014) Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat. Biotechnol., 32, 670-676.
31. Gagnon, J.A., Valen, E., Thyme, S.B., Huang, P., Akhmetova, L., Pauli, A., Montague, T.G., Zimmerman, S., Richter, C. and Schier, A.F. (2014) Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS One, 9, e98186.
32. Wang, T., Wei, J.J., Sabatini, D.M. and Lander, E.S. (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science, 343, 80-84.
33. Rink, T.J., Tsien, R.Y. and Pozzan, T. (1982) Cytoplasmic pH and free Mg2+ in lymphocytes. J. Cell Biol., 95, 189-196.
34. Semenova, E., Jore, M.M., Datsenko, K.A., Semenova, A., Westra, E.R., Wanner, B., van der Oost, J., Brouns, S.J. and Severinov, K. (2011) Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc. Natl. Acad. Sci. U.S.A., 108, 10098-10103.
35. Sternberg, S.H., Redding, S., Jinek, M., Greene, E.C. and Doudna, J.A. (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, 507, 62-67.
36. Fu, Y., Foden, J.A., Khayter, C., Maeder, M.L., Reyon, D., Joung, J.K. and Sander, J.D. (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol., 31, 822-826.
37. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T., Yeh, J.R. and Joung, J.K. (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol., 31, 227-229.
38. Pattanayak, V., Lin, S., Guilinger, J.P., Ma, E., Doudna, J.A. and Liu, D.R. (2013) High-throughput profiling of off-target DNA cleavage reveals RNAprogrammed Cas9 nuclease specificity. Nat. Biotechnol., 31, 839-843.
39. Hagedorn, M., Kleinhans, F.W., Artemov, D. and Pilatus, U. (1998) Characterization of a major permeability barrier in the zebrafish embryo. Biol. Reprod., 59, 1240-1250.
40. Priami, C. and Morine, M.J. (2015) Analysis of Biological Systems, Imperial College Press, London.
41. Record, M.T., Mazur, S. J., Melaqon, P., Roe, J.H., Shaner, S.L. and Unger, L. (1981) Double helical DNA: conformations, physical properties, and interactions with ligands. Annu. Rev. Biochem., 50, 997-1024.
42. Leirmo, S., Harrison, C., Cayley, D.S., Burgess, R.R. and Record, M.T. (1987) Replacement of potassium chloride by potassium glutamate dramatically enhances protein-DNA interactions in vitro. Biochemistry, 26, 2095-2101.
43. Lodish, H., Berk, A., Zipursky, S., Matsudaira, P., Baltimore, D. and Darnell, J. (2000) Molecular Cell Biology, W.H. Freeman, NY.
44. Kim, S., Kim, D., Cho, S.W., Kim, J. and Kim, J.S. (2014) Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res., 24, 1012-1019.
45. Dang, Y., Jia, G., Choi, J., Ma, H., Anaya, E., Ye, C., Shankar, P. and Wu, H. (2015) Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency. Genome Biol., 16, 280.