Mechanism of foreign DNA recognition by a CRISPR RNA-guided surveillance complex from Pseudomonas aeruginosa

Nucleic Acids Research

Volumn 43, Issue 4, 2015, Pages 2216-2222

  Rollins, Maryclare F ^a   Schuman, Jason T ^b   Paulus, Kirra ^a   Bukhari, Habib S T ^c   Wiedenheft, Blake ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b GE Healthcare Life Sciences   (United States)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; CRISPR ASSOCIATED PROTEIN; DNA; PROTEIN BINDING; SINGLE STRANDED DNA;

CHEMISTRY; CRISPR CAS SYSTEM; GENETICS; METABOLISM; NUCLEOTIDE MOTIF; PSEUDOMONAS AERUGINOSA;

CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DNA; DNA, SINGLE-STRANDED; NUCLEOTIDE MOTIFS; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; RNA, BACTERIAL;

EID: 84941061778     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv094     Document Type: Article

References (41)

1. Sorek, R., Lawrence, C.M., Wiedenheft, B. (2013) CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem., 82, 237-266.
2. Barrangou, R., Marraffini, L.A. (2014) CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol. Cell, 54, 234-244.
3. Wiedenheft, B., Sternberg, S.H., Doudna, J.A. (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature, 482, 331-338.
4. Bondy-Denomy, J., Davidson, A.R. (2014) To acquire or resist: the complex biological effects of CRISPR|Cas systems. Trends Microbiol., 22, 218-225.
5. 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.
6. Heler, R., Marraffini, L.A., Bikard, D. (2014) Adapting to new threats: the generation of memory by CRISPR-Cas immune systems. Mol. Microbiol., 93, 1-9.
7. 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.
8. 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.
9. 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.
10. Hale, C.R., Cocozaki, A., Li, H., Terns, R.M., Terns, M.P. (2014) Target RNA capture and cleavage by the Cmr type III-B CRISPR-Cas effector complex. Genes Dev., 28, 2432-2443.
11. Tamulaitis, G., Kazlauskiene, M., Manakova, E., Venclovas, C., Nwokeoji, A.O., Dickman, M.J., Horvath, P., Siksnys, V. (2014) Programmable RNA shredding by the Type III-A CRISPR-Cas system of Streptococcus thermophilus. Mol. Cell, 56, 506-517.
12. Benda, C., Ebert, J., Scheltema, R.A., Schiller, H.B., Baumgärtner, M., Bonneau, F., Mann, M., Conti, E. (2014) Structural model of a CRISPR RNA-silencing complex reveals the RNA-target cleavage activity in Cmr4. Mol. cell, 56, 43-54.
13. 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.
14. 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.
15. Sinkunas, T., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P., Siksnys, V. (2011) Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system. EMBO J., 30, 1335-1342.
16. 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.
17. 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.
18. 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.
19. Gasiunas, G., Barrangou, R., Horvath, P., 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.
20. 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.
21. Horvath, P., Coute-Monvoisin, A.C., Romero, D.A., Boyaval, P., Fremaux, C., Barrangou, R. (2008) Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int. J. Food Microbiol., 131, 62-70.
22. Mojica, F.J., Diez-Villasenor, C., Garcia-Martinez, J., Almendros, C. (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology, 155, 733-740.
23. 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, 1629-1638.
24. Sternberg, S.H., Redding, S., Jinek, M., Greene, E.C., Doudna, J.A. (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, 507, 62-67.
25. Anders, C., Niewoehner, O., Duerst, A., Jinek, M. (2014) Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature, 513, 569-573.
26. Hochstrasser, M.L., Taylor, D.W., Bhat, P., Guegler, C.K., Sternberg, S.H., Nogales, E., 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.
27. Wiedenheft, B., van Duijn, E., Bultema, J., Waghmare, S., Zhou, K., Barendregt, A., Westphal, W., Heck, A., Boekema, E., Dickman, M. 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.
28. Lee, D.G., Urbach, J.M., Wu, G., Liberati, N.T., Feinbaum, R.L., Miyata, S., Diggins, L.T., He, J., Saucier, M., Deziel, E. et al. (2006) Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol., 7, R90.
29. Cady, K.C., Bondy-Denomy, J., Heussler, G.E., Davidson, A.R., O'Toole, G.A. (2012) The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol., 194, 5728-5738.
30. Bondy-Denomy, J., Pawluk, A., Maxwell, K.L., Davidson, A.R. (2013) Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature, 493, 429-U181.
31. Wiedenheft, B. (2013) In defense of phage: viral suppressors of CRISPR-mediated adaptive immunity in bacteria. RNA Biol., 10, 886-890.
32. Bauer, M., Metzler, R. (2012) Generalized facilitated diffusion model for DNA-binding proteins with search and recognition states. Biophys. J., 102, 2321-2330.
33. Hu, L., Grosberg, A.Y., Bruinsma, R. (2008) Are DNA transcription factor proteins maxwellian demons? Biophys. J., 95, 1151-1156.
34. Zhou, H.X. (2011) Rapid search for specific sites on DNA through conformational switch of nonspecifically bound proteins. Proc. Natl. Acad. Sci. U.S.A., 108, 8651-8656.
35. Slutsky, M., Mirny, L.A. (2004) Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential. Biophys. J., 87, 4021-4035.
36. Matos, R.G., Barbas, A., Arraiano, C.M. (2010) Comparison of EMSA and SPR for the characterization of RNA-RNase II complexes. Protein J., 29, 394-397.
37. 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.
38. 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.
39. Wiedenheft, B., Lander, G.C., Zhou, K., Jore, M.M., Brouns, S.J.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.
40. 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.
41. 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.