CRISPR RNA binding and DNA target recognition by purified Cascade complexes from Escherichia coli

Nucleic Acids Research

Volumn 43, Issue 1, 2015, Pages 530-543

  Beloglazova, Natalia ^a   Kuznedelov, Konstantin ^b   Flick, Robert ^a   Datsenko, Kirill A ^c   Brown, Greg ^a   Popovic, Ana ^a   Lemak, Sofia ^a   Semenova, Ekaterina ^b   Severinov, Konstantin ^b,d   Yakunin, Alexander F ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b RUTGERS UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

^d INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DNA; ESCHERICHIA COLI PROTEIN; GUIDE RNA; PROTEIN BINDING;

CHEMISTRY; CRISPR CAS SYSTEM; ISOLATION AND PURIFICATION; METABOLISM;

CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DNA; ESCHERICHIA COLI PROTEINS; PROTEIN BINDING; RNA, GUIDE;

EID: 84942079467     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1285     Document Type: Article

References (52)

1. Makarova, K.S., Grishin, N.V., Shabalina, S.A., Wolf, Y.I., Koonin, E.V. (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct, 1, 7-33.
2. Makarova, K.S., Haft, D.H., Barrangou, R., Brouns, S.J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F.J., Wolf, Y.I., Yakunin, A.F. et al. (2011) Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol., 9, 467-477.
3. Bhaya, D., Davison, M., Barrangou, R. (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet., 45, 273-297.
4. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A., Horvath, P. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315, 1709-1712.
5. Hale, C.R., Zhao, P., Olson, S., Duff, M.O., Graveley, B.R., Wells, L., Terns, R.M., Terns, M.P. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell, 139, 945-956.
6. Westra, E.R., Swarts, D.C., Staals, R.H., Jore, M.M., Brouns, S.J., van der Oost, J. (2012) The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet., 46, 311-339.
7. 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., van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321, 960-964.
8. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
9. Garneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadan, A.H., Moineau, S. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 468, 67-71.
10. Haft, D.H., Selengut, J., Mongodin, E.F., Nelson, K.E. (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol., 1, e60.
11. Carte, J., Wang, R., Li, H., Terns, R.M., Terns, M.P. (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev., 22, 3489-3496.
12. Hatoum-Aslan, A., Maniv, I., Marraffini, L.A. (2011) Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc. Natl. Acad. Sci. U.S.A., 108, 21218-21222.
13. 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.
14. Semenova, E., Jore, M.M., Datsenko, K.A., Semenova, A., Westra, E.R., Wanner, B., van der Oost, J., Brouns, S.J., 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.
15. Wiedenheft, B., van Duijn, E., Bultema, J.B., Waghmare, S.P., Zhou, K., Barendregt, A., Westphal, W., Heck, A.J., Boekema, E.J., Dickman, M.J. et al. (2011) RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. U.S.A., 108, 10092-10097.
16. Savitskaya, E., Semenova, E., Dedkov, V., Metlitskaya, A., Severinov, K. (2013) High-throughput analysis of type I-E CRISPR/Cas spacer acquisition in E. coli. RNA Biol., 10, 716-725.
17. Yosef, I., Goren, M.G., Qimron, U. (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res., 40, 5569-5576.
18. Sorek, R., Lawrence, C.M., Wiedenheft, B. (2013) CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem., 82, 237-266.
19. Wiedenheft, B., Lander, G.C., Zhou, K., Jore, M.M., Brouns, S.J., van der Oost, J., Doudna, J.A., Nogales, E. (2011) Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature, 477, 486-489.
20. Westra, E.R., van Erp, P.B., Kunne, T., Wong, S.P., Staals, R.H., Seegers, C.L., 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.
21. Mulepati, S., 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.
22. Sinkunas, T., Gasiunas, G., Waghmare, S.P., Dickman, M.J., Barrangou, R., Horvath, P., Siksnys, V. (2013) In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J., 32, 385-394.
23. Jackson, R.N., Golden, S.M., van Erp, P.B., Carter, J., Westra, E.R., Brouns, S.J., van der Oost, J., Terwilliger, T.C., Read, R.J., Wiedenheft, B. (2014) Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli. Science, 345, 1473-1479.
24. Zhao, H., Sheng, G., Wang, J., Wang, M., Bunkoczi, G., Gong, W., Wei, Z., Wang, Y. (2014) Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli. Nature, 515, 147-150.
25. Mulepati, S., Heroux, A., Bailey, S. (2014) Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science, 345, 1479-1484.
26. Rouillon, C., Zhou, M., Zhang, J., Politis, A., Beilsten-Edmands, V., Cannone, G., Graham, S., Robinson, C.V., Spagnolo, L., White, M.F. (2013) Structure of the CRISPR interference complex CSM reveals key similarities with cascade. Mol. Cell, 52, 124-134.
27. Staals, R.H., Agari, Y., Maki-Yonekura, S., Zhu, Y., Taylor, D.W., van Duijn, E., Barendregt, A., Vlot, M., Koehorst, J.J., Sakamoto, K. et al. (2013) Structure and activity of the RNA-targeting Type III-B CRISPR-Cas complex of Thermus thermophilus. Mol. Cell, 52, 135-145.
28. Spilman, M., Cocozaki, A., Hale, C., Shao, Y., Ramia, N., Terns, R., Terns, M., Li, H., Stagg, S. (2013) Structure of an RNA silencing complex of the CRISPR-Cas immune system. Mol. Cell, 52, 146-152.
29. Marraffini, L.A., Sontheimer, E.J. (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science, 322, 1843-1845.
30. Zhang, J., Rouillon, C., Kerou, M., Reeks, J., Brugger, K., Graham, S., Reimann, J., Cannone, G., Liu, H., Albers, S.V. et al. (2012) Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol. Cell, 45, 303-313.
31. Juranek, S., Eban, T., Altuvia, Y., Brown, M., Morozov, P., Tuschl, T., Margalit, H. (2012) A genome-wide view of the expression and processing patterns of Thermus thermophilus HB8 CRISPR RNAs. RNA, 18, 783-794.
32. Haurwitz, R.E., Jinek, M., Wiedenheft, B., Zhou, K., Doudna, J.A. (2010) Sequence-and structure-specific RNA processing by a CRISPR endonuclease. Science, 329, 1355-1358.
33. Lintner, N.G., Kerou, M., Brumfield, S.K., Graham, S., Liu, H., Naismith, J.H., Sdano, M., Peng, N., She, Q., Copie, V. et al. (2011) Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE). J. Biol. Chem., 286, 21643-21656.
34. Sokolowski, R.D., Graham, S., White, M.F. (2014) Cas6 specificity and CRISPR RNA loading in a complex CRISPR-Cas system. Nucleic Acids Res., 42, 6532-6541.
35. Datsenko, K.A., 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.
36. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J.V., Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc., 1, 2856-2860.
37. Lemak, S., Beloglazova, N., Nocek, B., Skarina, T., Flick, R., Brown, G., Popovic, A., Joachimiak, A., Savchenko, A., Yakunin, A.F. (2013) Toroidal structure and DNA cleavage by the CRISPR-associated [4Fe-4S] cluster containing Cas4 nuclease SSO0001 from Sulfolobus solfataricus. J. Am. Chem. Soc., 135, 17476-17487.
38. Plagens, A., Tripp, V., Daume, M., Sharma, K., Klingl, A., Hrle, A., Conti, E., Urlaub, H., Randau, L. (2014) In vitro assembly and activity of an archaeal CRISPR-Cas type I-A Cascade interference complex. Nucleic Acids Res., 42, 5125-5138.
39. Sternberg, S.H., Haurwitz, R.E., Doudna, J.A. (2012) Mechanism of substrate selection by a highly specific CRISPR endoribonuclease. RNA, 18, 661-672.
40. Niewoehner, O., Jinek, M., Doudna, J.A. (2014) Evolution of CRISPR RNA recognition and processing by Cas6 endonucleases. Nucleic Acids Res., 42, 1341-1353.
41. van der Oost, J., Westra, E.R., Jackson, R.N., Wiedenheft, B. (2014) Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat Rev Microbiol, 12, 479-492.
42. Deveau, H., Barrangou, R., Garneau, J.E., Labonte, J., Fremaux, C., Boyaval, P., Romero, D.A., Horvath, P., Moineau, S. (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol., 190, 1390-1400.
43. Martel, B., Moineau, S. (2014) CRISPR-Cas: an efficient tool for genome engineering of virulent bacteriophages. Nucleic Acids Res., 42, 9504-9513.
44. Szczelkun, M.D., Tikhomirova, M.S., Sinkunas, T., Gasiunas, G., Karvelis, T., Pschera, P., Siksnys, V., 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.
45. Ivancic-Bace, I., Howard, J.A., Bolt, E.L. (2012) Tuning in to interference: R-loops and cascade complexes in CRISPR immunity. J. Mol. Biol., 422, 607-616.
46. Sasse-Dwight, S., Gralla, J.D. (1989) KMnO4 as a probe for lac promoter DNA melting and mechanism in vivo. J. Biol. Chem., 264, 8074-8081.
47. Westra, E.R., Semenova, E., Datsenko, K.A., Jackson, R.N., Wiedenheft, B., Severinov, K., Brouns, S.J. (2013) Type I-E CRISPR-cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition. PLoS Genet., 9, e1003742.
48. Fineran, P.C., Gerritzen, M.J., Suarez-Diez, M., Kunne, T., Boekhorst, J., van Hijum, S.A., Staals, R.H., Brouns, S.J. (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl. Acad. Sci. U.S.A., 111, E1629-E1638.
49. Sashital, D.G., Jinek, M., Doudna, J.A. (2011) An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat. Struct. Mol. Biol., 18, 680-687.
50. Wiedenheft, B., Sternberg, S.H., Doudna, J.A. (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature, 482, 331-338.
51. Carte, J., Christopher, R.T., Smith, J.T., Olson, S., Barrangou, R., Moineau, S., Glover, C.V. 3rd, Graveley, B.R., Terns, R.M., Terns, M.P. (2014) The three major types of CRISPR-Cas systems function independently in CRISPR RNA biogenesis in Streptococcus thermophilus. Mol. Microbiol., 93, 98-112.
52. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J., Charpentier, E. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 471, 602-607.