CRISPR interference and priming varies with individual spacer sequences

Nucleic Acids Research

Volumn 43, Issue 22, 2015, Pages 10831-10847

  Xue, Chaoyou ^a   Seetharam, Arun S ^a   Musharova, Olga ^b,c,d   Severinov, Konstantin ^b,c,d,e   Brouns, Stan J J ^f   Severin, Andrew J ^a   Sashital, Dipali G ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^c SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

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

^e RUTGERS UNIVERSITY   (United States)

^f WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; CRISPR CAS SYSTEM; ESCHERICHIA COLI; FEEDBACK SYSTEM; GENOMICS; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTOSPACER ADJACENT MOTIF; RNA INTERFERENCE; BACTERIAL GENOME; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; ENZYMOLOGY; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MUTATION;

CRISPR ASSOCIATED PROTEIN; DEOXYRIBONUCLEASE; ESCHERICHIA COLI PROTEIN;

CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOME, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MUTATION;

EID: 84959407493     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1259     Document Type: Article

References (66)

1. Barrangou, R. and Marraffini, L.A. (2014) CRISPR-Cas systems: Prokaryotes upgrade to adaptive immunity. Mol. Cell, 54, 234-244.
2. van der Oost, J., Westra, E.R., Jackson, R.N. and Wiedenheft, B. (2014) Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat. Rev. Microbiol., 12, 479-92.
3. Heler, R., Marraffini, L.A. and Bikard, D. (2014) Adapting to new threats: The generation of memory by CRISPR-Cas immune systems. Mol. Microbiol., 93, 1-9.
4. Kiro, R., Goren, M.G., Yosef, I. and Qimron, U. (2013) CRISPR adaptation in Escherichia coli subtypeI-E system. Biochem. Soc. Trans., 41, 1412-1415.
5. Hochstrasser, M.L. and Doudna, J.A. (2015) Cutting it close: CRISPR-associated endoribonuclease structure and function. Trends Biochem. Sci., 40, 58-66.
6. Charpentier, E., Richter, H., van der Oost, J. and White, M.F. (2015) Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity. FEMS Microbiol. Rev., 39, 428-441.
7. Jackson, R.N. and Wiedenheft, B. (2015) A conserved structural chassis for mounting versatile CRISPR RNA-guided immune responses. Mol. Cell, 58, 722-728.
8. Plagens, A., Richter, H., Charpentier, E. and Randau, L. (2015) DNA and RNA interference mechanisms by CRISPR-Cas surveillance complexes. FEMS Microbiol. Rev., 39, 442-463.
9. 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. (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol., 13, 722-736.
10. Yosef, I., Goren, M.G. and Qimron, U. (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res., 40, 5569-5576.
11. Datsenko, K.A., Pougach, K., Tikhonov, A., Wanner, B.L., Severinov, K. and Semenova, E. (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun., 3, 945.
12. Nuñez, J.K., Kranzusch, P.J., Noeske, J., Wright, A.V., Davies, C.W. and Doudna, J.a (2014) Cas1-Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nat. Struct. Mol. Biol., 21, 528-534.
13. Nunez, J.K., Lee, A.S.Y., Engelman, A. and Doudna, J.A. (2015) Integrase-mediated spacer acquisition during CRISPR-Cas adaptive immunity. Nature, 519, 193-198.
14. 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. and van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321, 960-964.
15. Hale, C.R., Zhao, P., Olson, S., Duff, M.O., Graveley, B.R., Wells, L., Terns, R.M. and Terns, M.P. (2009) RNA-Guided RNA Cleavage by a CRISPR RNA-Cas Protein Complex. Cell, 139, 945-956.
16. Hatoum-Aslan, A., Samai, P., Maniv, I., Jiang, W. and Marraffini, L.A. (2013) A ruler protein in a complex for antiviral defense determines the length of small interfering CRISPR RNAs. J. Biol. Chem., 288, 27888-27897.
17. 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.
18. Gasiunas, G., Barrangou, R., Horvath, P. and Siksnys, V. (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. U.S.A., 109, E2579-E2586.
19. 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. (2015) Cpf1 Is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 163, 759-771.
20. Shmakov, S., Abudayyeh, O.O., Makarova, K.S., Wolf, Y.I., Gootenberg, J.S., Semenova, E., Minakhin, L., Joung, J., Konermann, S., Severinov, K. et al. (2015) Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol. Cell, doi:10.1016/j.molcel.2015.10.008.
21. 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.
22. Jackson, R.N., Golden, S.M., van Erp, P.B.G., Carter, J., Westra, E.R., Brouns, S.J.J., van der Oost, J., Terwilliger, T.C., Read, R.J. and Wiedenheft, B. (2014) Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli. Science, 345, 1473-1479.
23. Mulepati, S., Héroux, A. and Bailey, S. (2014) Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science, 345, 1479-1484.
24. Zhao, H., Sheng, G., Wang, J., Wang, M., Bunkoczi, G., Gong, W., Wei, Z. and Wang, Y. (2014) Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli. Nature, 515, 147-150.
25. Mulepati, S. and Bailey, S. (2013) In vitro reconstitution of an Escherichia coli RNA-guided immune system reveals unidirectional, ATP-dependent degradation of DNA Target. J. Biol. Chem., 288, 22184-22192.
26. Westra, E.R., van Erp, P.B.G., Künne, T., Wong, S.P., Staals, R.H.J., Seegers, C.L.C., Bollen, S., Jore, M.M., Semenova, E., Severinov, K. et al. (2012) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by cascade and Cas3. Mol. Cell, 46, 595-605.
27. Hochstrasser, M.L., Taylor, D.W., Bhat, P., Guegler, C.K., Sternberg, S.H., Nogales, E. and Doudna, J.a (2014) CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. Proc. Natl. Acad. Sci. U.S.A., 111, 6618-6623.
28. Swarts, D.C., Mosterd, C., van Passel, M.W.J. and Brouns, S.J.J. (2012) CRISPR interference directs strand specific spacer acquisition. PLoS One, 7, e35888.
29. Yosef, I., Shitrit, D., Goren, M.G., Burstein, D., Pupko, T. and Qimron, U. (2013) DNA motifs determining the efficiency of adaptation into the Escherichia coli CRISPR array. Proc. Natl. Acad. Sci. U.S.A., 110, 14396-14401.
30. Sashital, D.G., Wiedenheft, B. and Doudna, J.A. (2012) Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol. Cell, 46, 606-615.
31. Semenova, E., Jore, M.M., Datsenko, K.A., Semenova, A., Westra, E.R., Wanner, B., van der Oost, J., Brouns, S.J.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.
32. Rollins, M.F., Schuman, J.T., Paulus, K., Bukhari, H.S.T. and Wiedenheft, B. (2015) Mechanism of foreign DNA recognition by a CRISPR RNA-guided surveillance complex from Pseudomonas aeruginosa. Nucleic Acids Res., 43, 2216-2222.
33. 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.
34. Rutkauskas, M., Sinkunas, T., Songailiene, I., Tikhomirova, M.S., Siksnys, V. and Seidel, R. (2015) Directional R-loop formation by the CRISPR-Cas surveillance complex cascade provides efficient off-target site rejection. Cell Rep., doi:10.1016/j.celrep.2015.01.067.
35. 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.
36. Fineran, P.C., Gerritzen, M.J.H., Suárez-Diez, M., Künne, T., Boekhorst, J., van Hijum, S.a F.T., Staals, R.H.J. and Brouns, S.J.J. (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl. Acad. Sci. U.S.A., 111, E1629-E1638.
37. Blosser, T.R., Loeff, L., Westra, E.R., Vlot, M., Kunne, T., Sobota, M., Dekker, C., Brouns, S.J.J. and Joo, C. (2015) Two distinct DNA binding modes guide dual roles of a CRISPR-Cas protein complex. Mol. Cell, 58, 60-70.
38. 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. Biotech., 31, 827-832.
39. 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 RNA-programmed Cas9 nuclease specificity. Nat. Biotech., 31, 839-843.
40. 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.
41. 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.
42. 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.
43. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A., 97, 6640-6645.
44. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K.A., Tomita, M., Wanner, B.L. and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol., 2, 2006.0008.
45. Cherepanov, P.P. and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene, 158, 9-14.
46. de Boer, H.A., Comstock, L.J. and Vasser, M. (1983) The tac promoter: a functional hybrid derived from the trp and lac promoters. Proc. Natl. Acad. Sci. U. S. A., 80, 21-25.
47. De Mey, M., Maertens, J., Lequeux, G.J., Soetaert, W.K. and Vandamme, E.J. (2007) Construction and model-based analysis of a promoter library for E. coli: an indispensable tool for metabolic engineering. BMC Biotechnol., 7, 34.
48. Keiler, K.C., Waller, P.R. and Sauer, R.T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science, 271, 990-993.
49. Gibson, D.G., Young, L., Chuang, R.-Y., Venter, J.C., Hutchison, C.A. 3rd and Smith, H.O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods, 6, 343-345.
50. Aronesty, E. (2013) Comparison of sequencing utility programs. Open Bioinforma. J., 7, 1-8.
51. Quinlan, A.R. (2014) BEDTools: the Swiss-Army tool for genome feature analysis. Curr. Protoc. Bioinformatics, 47, 11.12.1-11.12.34.
52. Westra, E.R., Pul, Ü., Heidrich, N., Jore, M.M., Lundgren, M., Stratmann, T., Wurm, R., Raine, A., Mescher, M., Van Heereveld, L. et al. (2010) H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO. Mol. Microbiol., 77, 1380-1393.
53. Edgar, R. and Qimron, U. (2010) The Escherichia coli CRISPR system protects from lambda lysogenization, lysogens, and prophage induction. J. Bacteriol., 192, 6291-6294.
54. Pougach, K., Semenova, E., Bogdanova, E., Datsenko, K.A., Djordjevic, M., Wanner, B.L. and Severinov, K. (2010) Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol. Microbiol., 77, 1367-1379.
55. Pul, Ü., Wurm, R., Arslan, Z., Geißen, R., Hofmann, N. andWagner, R. (2010) Identification and characterization of E. coli CRISPR-Cas promoters and their silencing by H-NS. Mol. Microbiol., 75, 1495-1512.
56. Savitskaya, E., Semenova, E., Dedkov, V., Metlitskaya, A. and Severinov, K. (2013) High-throughput analysis of type I-E CRISPR/Cas spacer acquisition in E. coli. RNA Biol., 10, 716-725.
57. Diez-Villasenor, C., Guzman, N.M., Almendros, C., Garcia-Martinez, J. and Mojica, F.J.M. (2013) CRISPR-spacer integration reporter plasmids reveal distinct genuine acquisition specificities among CRISPR-Cas I-E variants of Escherichia coli. RNA Biol., 10, 792-802.
58. Westra, E.R., Semenova, E., Datsenko, K.A., Jackson, R.N., Wiedenheft, B., Severinov, K. and Brouns, S.J.J. (2013) Type I-E CRISPR-Cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition. PLoS Genet., 9, e1003742.
59. Semenova, E., Kuznedelov, K., Datsenko, K.A., Boudry, P.M., Savitskaya, E.E., Medvedeva, S., Beloglazova, N., Logacheva, M., Yakunin, A.F. and Severinov, K. (2015) The Cas6e ribonuclease is not required for interference and adaptation by the E. coli type I-E CRISPR-Cas system. Nucleic Acids Res., 43, 6049-6061.
60. Marraffini, L.A. and Sontheimer, E.J. (2010) Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature, 463, 568-571.
61. Li, M., Wang, R. and Xiang, H. (2014) Haloarcula hispanica CRISPR authenticates PAM of a target sequence to prime discriminative adaptation. Nucleic Acids Res., 42, 7226-7235.
62. Wang, J., Li, J., Zhao, H., Sheng, G., Wang, M., Yin, M. and Wang, Y. (2015) Structural and mechanistic basis of PAM-dependent spacer acquisition in CRISPR-Cas systems. Cell, doi:10.1016/j.cell.2015.10.008.
63. Kupczok, A. and Bollback, J.P. (2014) Motif depletion in bacteriophages infecting hosts with CRISPR systems. BMC Genomics, 15, 663.
64. Li, M., Wang, R., Zhao, D. and Xiang, H. (2014) Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res., 42, 2483-2492.
65. Richter, C., Dy, R.L., McKenzie, R.E., Watson, B.N.J., Taylor, C., Chang, J.T., McNeil, M.B., Staals, R.H.J. and Fineran, P.C. (2014) Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer. Nucleic Acids Res., 42, 8516-8526.
66. Levy, A., Goren, M.G., Yosef, I., Auster, O., Manor, M., Amitai, G., Edgar, R., Qimron, U. and Sorek, R. (2015) CRISPR adaptation biases explain preference for acquisition of foreign DNA. Nature, 520, 505-510.